A Wikiblog E-Book by Norman Uphoff with many others
Chapter 5: CONTRIBUTIONS FROM THE LIFE IN THE SOIL
Experience and research with SRI have underscored some important parallels between plant science and the study of human biology. Increasingly, it is recognized that humans are not self-sufficient organisms because our species Homo sapiens, like other animals, is thoroughly interactive with and dependent upon the uncountable species and numbers of microorganisms that live around, on, and even within us.
Humans function essentially as complex systems of diverse, interdependent living cells. Similarly, plants are more than just plant. They function as superorganisms that coexist with the myriad microbes that surround and inhabit them. The genetic capabilities and potentials of the microorganisms that are intimately associated with plants are collectively referred to as the plant’s microbiome. This provides plants with benefits and services akin to those that human microbiomes bestow upon us.
Diverse populations of bacteria, fungi and other microbes perform many functions for plants, promoting plants’ growth through the cycling and provision of nutrients and the production of plant growth hormones (phytohormones). Various microbial species fix nitrogen, solubilize phosphorus, and decompose organic matter to make its carbon and nutrients plant-available. They also synthesize antibiotic compounds that control pathogens, and they can induce within plants systemic resistance to pests and diseases.
Microbes can confer stress tolerance on plants through molecular pathways that are becoming better understood, and they both produce and reduce greenhouse gas emissions. As many as 1,000 species of microorganisms live in the soil around plants’ roots, known as the rhizosphere, and on the above-ground surfaces of plants that constitute the phyllosphere. Many more bacteria and fungi reside inside plant tissues and even inside cells as what are called symbiotic endophytes, the latter word meaning ‘within plants.’
For many years, the study of microbes in, on and around plants looked upon microorganisms in adversarial terms, reflected in the name given to the discipline of plant pathology, which focused on the ‘bad guys’ in the microbial realm. Fortunately in recent years the preoccupation with disease and parasitism has given way to more analysis of mutualism and the symbiotic existence that is beneficial for both the plants and microbes that interact.
It was timely that our efforts to understand the sources of SRI began about the same time that research into mutually-advantageous plant-microbial relationships began accelerating. There was already some general understanding of the importance of microbes for rice plants’ growth and performance. But soil biology was largely ignored by rice breeders and was not much given thought by agronomists.
In some ways, we have been re-learning with SRI what farmers have known for a long time, that fertile soil is more than just the minerals available within it. Fertile soil is living soil, containing within its material matrix a vast but mostly unseen array of organisms. Productive soil is generally, by volume, only about half mineral. This is the visible, inert and solid portion of soil that can be bought and owned, tilled and eroded.
About as much of the soil’s volume, if it is well-structured and not compacted, will be the water and air that circulate within its vast network of pore spaces. Three to five percent of the total volume of soil, and often much less, will be organic matter, dead and alive. Speaking metaphorically, this is the tail that wags the dog. But the relationship between soil organisms and the soil and plants which they inhabit and benefit is not one-way. Plants through biochemicals exuded from their roots influence the composition as well as the abundance of microbes that surround and service them.
As this story is about SRI, not soil science, these matters will not be elaborated. But some consideration of soils and soil biology will necessarily be part of the discussion as we proceed because SRI is a strategy based on a synthesis of better ways to manage plants, soil, water, and nutrients all together, along with all the organisms that reside within the soil system and within plants.
Soil systems, which are more than just ‘soil,’ are active rather than a passive participants in the SRI production process. Our comprehension of this started with the wise counsel of Prof. Robert Randriamiharisoa who was at the time director of research for the Faculty of Agriculture at the University of Antananarivo in Madagascar. Prof. Robert was introduced in the preceding chapter as an initial contributor to our construction of a scientifically-grounded understanding of SRI.
RICE PLANTS BENEFIT FROM BACTERIA BOTH IN THEIR ROOT ZONES AND ROOTS
Most people know that there are some members of the plant kingdom, classified as legumes, which benefit from a symbiotic relationship with certain species of bacteria, rhizobia, that live in the soil and also in plants. These microorganisms induce and inhabit nodules that form on leguminous plants’ roots through an intricate process of signaling and accommodation between the plant and these resident bacteria.
Rhizobia are said to be ‘fixing’ nitrogen (N) when they convert this element from its gaseous form (N₂), abundantly available in the atmosphere, into the compound ammonia (NH₃). Atmospheric nitrogen makes up 78% of the air around us, but plants cannot take up and utilize nitrogen in this elemental form. The activity and intermediation of microbes is needed for plants to be supplied with useable nitrogen.
That leguminous plants, thanks to symbiotic microbes, fix nitrogen for themselves while also building up N reserves in the soil has seemed to imply that the soils in which non-leguminous crops are grown must be enhanced with exogenous N fertilizer because such crops lack the capability to transform N₂ into NH₃. However, this turns out to be wrong. That rice is not a legume with N-fixing nodules on its roots does not make it any less interdependent on the activities and services of the life in the soil.
When Glenn Lines and I met with Prof. Robert in his office in March 1997, we discussed what plant nutrition was needed to achieve and sustain the high rice yields that Ranomafana farmers were getting when using SRI practices. Both Glenn and I knew that soya beans and other legumes, including fast-growing leguminous trees, can fix nitrogen through microbial activity in their root nodules that benefits themselves and others. Prof. Robert explained to us how some crops including rice which are not legumes benefit from free-living, aerobic bacteria that reside around, on, and even inside plants, fixing nitrogen and providing other services.
These organisms, instead of living within nodules which are a special feature of legumes, live in close proximity with plant roots or within roots. They benefit the associated plants while they are themselves supported by exudates from the plant roots: carbohydrates, amino acids, and other compounds emitted into the soil. Those organisms that live within plant roots get their nourishment directly. Prof. Robert’s explanation prompted me to bring on my next trip to Madagascar a book by the Brazilian agronomist Johanna Döbereiner as airplane reading. The more that I learned about the symbiotic relationships between plants and microbes, the more promising this line of investigation appeared.
FUNGI ALSO CONTRIBUTE TO SRI SUCCESS
Because most beneficial soil microbes are aerobic, needing oxygen for their survival, SRI’s water management, by permitting oxygen to get into the rhizosphere soil around plant roots, opens opportunities for supportive microbial activity that is subdued by standard rice cultivation methods. When the continuous flooding of rice paddies is halted, rice plants benefit from the services not only of bacteria but also of fungi in the soil and plant roots. Fungi, a vast kingdom of microorganisms that need oxygen to survive, improve soil structure, enhance water dynamics, assist in nutrient cycling, decompose organic matter in the soil, and suppress diseases.
The changes that SRI makes in water management are particularly important for their effect on what are called mycorrhizal fungi. These are a diversity of fungal species that inhabit the roots of over 80% of terrestrial plant species, sending out long microscopic filaments (hyphae) into the soil. In a cubic centimeter of soil, the total length of such hyphae can add up to over 100 meters, something difficult to comprehend but well-known to those who study these organisms.
The invisible thread-like hyphal extensions of mycorrhizal fungi living in plant roots greatly expand the ability of root systems to take up water and nutrients from the surrounding soil. In return, these fungi receive energy (carbohydrates) from the plant in a symbiotic relationship.
The fossil record shows that these mutually beneficial relations between plants and fungi go back more than 400 million years. Because fungi are oxygen-dependent, the flooding of rice fields deprives rice plants of the benefits that they can get from having mycorrhizal fungi residing in their roots. By inhabiting rice plant’s roots and extending their networks of hyphae up to 10 cm or more into the soil, mycorrhizal fungi give rice root systems access to what is in a greatly increased volume of soil, particularly enhancing the uptake of phosphorus.
That SRI practices create soil conditions favorable to rice roots’ being inhabited by mycorrhizal fungi can in itself explain part of the improved growth and health observed in SRI rice plants. But knowledge extrapolated from the literature was not sufficient. To understand what was going on within rice plants that was contributing to positive SRI results, we needed to have some direct evidence.
As discussed toward the end of this chapter, the first published evidence of symbiotic relationships between beneficial fungi and SRI management practices have focused on the effects of the fungal genus Trichoderma. But the first evidence of positive effects attributable to microorganisms conjoined with SRI practices was seen with a bacterium known as Azospirillum as part of the first experimental evaluations of SRI effects done in Madagascar.
AN ASSOCIATION BETWEEN SRI AND GROWTH-PROMOTING BACTERIA
In 2001, we got the first experimental confirmation that SRI practices affect the abundance of bacteria that live in rice plant roots and contribute to rice plants’ success. As part of the large set of factorial trials which are discussed in Chapter 7, a top agronomy student at the University of Antananarivo under Prof. Robert’s supervision, Andry Andriankaja, included in the design of his thesis research a component evaluating the effects of the diazotrophic (nitrogen-fixing) bacterium Azospirillum in response to SRI management. 
Azospirillum was chosen for study because it is well described in the literature, is known to fix nitrogen, and could be counted reasonably reliably in the lab of the Pasteur Institute in Antananarivo. It was not assumed that Azospirillum was the only microbial species involved in beneficial interactions with rice plants, but that it would be representative of what happens with microbial populations under the particular soil, water and nutrient management conditions of SRI compared with conventional practice.
The results reported below are from replicated trials, using appropriate sampling methods in the respective plots, comparing farmer practices and SRI practices when growing the same variety of rice on two different kinds of soil. The test plots were laid out with randomized block design on farmers’ fields near Anjomakely in the highlands of Madagascar, at about 1200 m elevation. Plant growth and yield were considered on both clay soil and loam soil because microbial populations and dynamics are known to be affected by soil differences.
Rice roots were dug up from the respective on-farm trial plots, washed, and then pulverized. The mashed-up samples were then examined under a microscope to count the numbers of colony forming units (CFUs), the standard unit for measuring numbers of viable bacterial or fungal cells. Comparisons were made in terms of the numbers of CFUs per milligram of root material that had been cleaned and crushed up. The numbers can be quite huge, and also very variable.
On the better clay soil, the use of farmer methods without any addition of nutrients to the plots resulted in rice plants that had on average 17 tillers and a harvested yield that amounted to 1.8 tonnes per hectare, about the national average. On the same soil, when SRI methods were used without any added nutrients, the number of tillers on each plant almost tripled, and the yield increased by more than three times.
Across all of the trials, there were no significant differences in the numbers of Azospirillum observed in the soil around the roots, the rhizosphere, which was a little surprising. However, it was very surprising that just by changing practices -- switching from older seedlings transplanted closely in flooded soil to young seedlings widely spaced in unflooded soil, all practices that promote greater root growth -- the numbers of Azospirillum living inside the roots dramatically multiplied, increasing more than 15-fold, and the associated grain yield more than tripled compared to farmer practice, without applying any fertilizer to the plots.
Adding fertilizer with nitrogen as well as some phosphorus and potassium in recommended doses for the particular soil increased the tillering of SRI plants by 50%, while it also added 50% to grain yield, reaching 9 tonnes per hectare. This was five times the level achieved with unfertilized farmer practices, a huge improvement. However, it was also seen that applying N fertilizer reduced the levels of Azospirillum inside the plant roots by 60%, to 450,000 per milligram. This meant that the higher grain yield achieved was being supported mostly by inorganic N, not by N that resulted from microbiological activity.
The addition of exogenous N fertilizer had a suppressive effect on the populations of Azospirillum in the rice roots. Possibly the abundance of inorganic N increased the populations of other microorganisms that competed successfully with Azospirillum for various nutrients in the soil, or the fertilizer lowered soil pH, increasing acidity. Certainly using fertilizer together with SRI practices was successful, but at the cost of inhibiting endogenous microbiological activity.
Probably the most important finding from the analysis was that when compost was added to SRI-managed plots instead of fertilizer, at a rate of just 5 tonnes per hectare, both tillering and yield further increased, by an additional 15-16%. And the numbers of Azospirillum resident in the roots sky-rocketed, to 1.1 million CFUs per mg, more than triple the number when the soil was amended with inorganic fertilizer.
The full set of treatments was not replicated on the less-fertile loamy soils; just two of the four treatments were evaluated, with all treatments replicated six times. When no nutrient amendments were made to loamy soil, SRI methods produced a respectable number of tillers (32), but the harvested yield was not much more, just 17%, than what farmers’ methods produced on the better clay soil. Neither were the numbers of Azospirillum in the plant roots much enhanced, just by 15% more.
However, when organic compost was added to this soil along with using SRI methods, grain production was boosted up to 6.6 tonnes per hectare, more than triple the usual rice yield in Madagascar. And this increase was supported by large populations of Azospirillum, 2 million CFUs per milligram of root mass, responding to the enhanced availability of organic material in the soil.
These numbers would surely vary across different trials since the dynamics of microorganisms’ growth and activity are very sensitive to changes in oxygenation, substrate, temperature, soil texture, structure, and other conditions. But the pattern of changes observed makes sense to anyone acquainted with microbial biology and ecology. These changes in microbial populations helped us make sense of the large differences that we were observing in rice plant productivity in farmers’ fields.
These results encouraged other researchers to look at how SRI management practices affect soil microbial populations. The table below summarizes results from studies done in India, at the Tamil Nadu Agricultural University (TNAU) and the International Crop Research Institute for the Semi-Arid Tropics (ICRISAT) and in Indonesia , at the Agricultural University at Bogor (IPB).
The trials compared microbial populations in rhizosphere soil samples around roots when rice plants of the same variety were grown on the same soils, with some trials using SRI methods and comparable trials using conventional practices. Unfortunately, they did not also assess microbes living symbiotically within the roots.
As with the data reported above, it should be remembered that when evaluating microbiological numbers and dynamics, one can expect a considerable range of values for the same variable. We need to be looking for patterns that can be interpreted since the numbers themselves can vary widely in response to changes in temperature, soil moisture, etc. The numbers below show the effects of SRI management practices on specific bacteria that increase the availability of nitrogen or phosphorus in the soil.
MICROBIAL ACTIVITY CAN ENHANCE THE AVAILABILITY OF PHOSPHORUS
Nitrogen is usually regarded as the main nutrient limiting the realization of crop yield potentials. It was encouraging to learn that certain nitrogen-fixing microorganisms living in association with rice roots can make N available to meet the crop’s nutritional needs, even if rice is not a leguminous plant that forms nodules on its roots for this purpose. But in Ranomafana we particularly needed to address the evident constraint of having exceedingly low levels of phosphorus (P) in the soils there.
Phosphorus is the second most critical nutrient needed for plant growth. Having abundant N available thanks to microbial activity will not help the plants very much if there is not also sufficient P available to support plant growth. Both of these macronutrients as well as dozens of micronutrients are needed for crop production to succeed.
Phosphorus is a nutrient much less freely available for plant use than is N, even though large stocks of P exist in most soils in ‘unavailable’ form that plants cannot access and benefit from. Most soils contain 10, 20, 30 times as much P tied up in insoluble compounds that roots cannot take up or in miniscule pore spaces that roots cannot enter, compared to the amounts that are dissolved in the water circulating within the soil system.
This water content in the soil is referred to as the soil solution, and it contains gases, organic matter, and minerals that roots can readily access. When certain soil is said to have ‘insufficient phosphorus,’ this usually refers to the amount of available P dissolved in the soil solution. This can be just a small percentage of the total P that is in the soil, however, as little as 0.1%. The fixation of N is beneficial for plants, as explained above, but it is not desirable for P to be fixed because this means that it is not available for plants’ use.
It turns out that biological processes can make unavailable P available through the activity of what are classified as phosphorus-solubilizing bacteria (PSB), noted in the table above. These aerobic microbes are capable of synthesizing and secreting organic compounds that dissolve ion bonds and break off chemical ions that contain P, e.g., phosphates (PO₄³⁻).
This phosphorus is utilized for the organisms’ own benefit, but it becomes available in the soil when these bacteria die and decompose. Such organisms are, in effect, ‘mining’ unavailable P in the soil and moving it into the soil’s pool of available phosphorus when the elements that had composed the deceased bacteria went into the soil solution. This process has been going on for hundreds of millions of years.
As reported in Chapter 3, an agronomy thesis for North Carolina State University on the soils around Ranomafana had concluded that their levels of (available) P were unprecedentedly low, only 3 to 4 parts per million (ppm). Agronomists generally consider 10 ppm to be the minimum required to get acceptable crop growth, and 30 to 50 ppm is generally considered to be a desirable range for P availability in the soil.
Thus, farmers in Ranomafana had only about 10% as much available phosphorus in their soil as they should have had for successful rice production. This widely-accepted guideline from standard soil science made it seem all the more inexplicable how these farmers by using SRI methods were producing four times their previous yield of paddy rice without buying and applying any phosphorus fertilizer!
In May 2001, as I was leaving for a trip to Madagascar, my wife Marguerite who has been a great help throughout this SRI story in so many ways, called to my attention a short article that she had noticed in a just-arrived issue of Nature magazine. The article was titled ‘Phosphorus Solubilization in Rewetted Soils.’
The article’s British authors had studied soils in 29 locations of England and Wales, taking soil samples and recording the samples’ levels of available P when the soils were wet or dry. “The total amounts of water-soluble phosphorus in moist soils were small, but [these amounts] increased after drying by 185-1,900%,” they wrote. Although available P was very limited in wet soils, it increased hugely when these soils were subsequently dried out.
This was one of the many ‘eureka’ moments in the SRI story. The data and interpretation presented by Turner and Haygarth could help to account for how the soils in Ranomafana, which according to standard scientific evaluation should be producing little if any crop, were in fact giving farmers remarkable increases in rice production. Phosphorous-solubilizing bacteria, being aerobic, could thrive and multiply in paddy soil during its dry phase if they had access to enough organic matter in the soil, i.e., enough carbon to provide them with energy.
Then when the soil was flooded (anaerobic), the PSBs would die because they require oxygen. When these microbial cells disintegrated and decomposed, the P they contained was released into the soil solution, from which plant roots could take it up. In their article, Turner and Haygarth speculated that this biologically-driven process, a by-product of their wetting and drying the soil samples, could similarly mobilize other soil nutrients, like micronutrients. This dynamic process was further examined and verified in subsequent research and publications.
Because Turner and Haygarth were working as environmental rather than as agricultural scientists, they did not look upon increases in phosphorus levels in the soil solution as being a good thing because it contributed to the eutrophication of water bodies. However, Turner became interested in the relevance of his finding for SRI and visited Madagascar to assess the soils there. He did not find as much effect of wetting and drying on phosphorus levels as he did in the U.K.
Fortunately, Ben did not give up his curiosity about SRI and about soil phosphorus dynamics. Subsequently he supervised PhD thesis research on this relationship when in Panama at the Smithsonian Institution’s Tropical Research Institute there. The different, more positive results in Panama were indicative of the complexity and frequent ambiguity of soil biology and ecological relationships, especially in the tropics with considerable temperature, humidity and other variability.
The thesis by Marie-Soleil Turmel included a meta-analysis of 72 field trials across 16 countries where SRI results had been compared with conventional methods. This was the most thorough comparative evaluation of SRI results than had been done with a focus on soil and nutrient effects. The analysis, published separately from the thesis, found that SRI methods on highly-weathered, infertile soils produced significant yield increases (P<.0001), whereas when they were employed on more fertile soils, there were SRI yield improvements, but not statistically significant.
When the trials were grouped according to their inherent soil fertility as classified by standard FAO criteria, the yields on the more fertile soils were, as expected, higher; but the SRI yield advantage was less. On soils of low, moderate and high fertility, average SRI yields were, respectively, 5.8, 7.0 and 7.7 tonnes per hectare, while the yields per hectare with conventional methods were 4.3, 6.1 and 7.4 tonnes. Thus, the yield advantages for the three categories were, respectively, 35%, 15% and 4%.
This suggested something quite unusual. It showed SRI to be an innovation that produces relatively greater benefit for farmers who have ‘poorer’ land and who are usually poor themselves. Giving relatively more opportunity to the poor than to the rich, who usually become richer by development innovations, was not anticipated.
In her thesis fieldwork in Panama with trials in 10 locations, Turmel found low soil fertility (low yields) to be closely associated with the low availability of phosphorus in the soil. Given the high acidity (low pH) of these soils, most of the total phosphorus in them was ‘fixed,’ i.e., unavailable for plant use. SRI’s water and nutrient management practices enhanced the availability of P though microbial activity that was supported by SRI’s more aerobic soil conditions and by the greater supply of organic material in the soil. Across the 10 locations, SRI methods were seen to increase average yield by 47% while reducing crop water requirements by 86%.
The possibility that phosphorus was being made more available in soils, particularly in acidic, low-fertility soils, by changes that SRI introduced in how water and nutrients are managed -- suggested ten years previously in that brief Nature magazine report -- was thus supported and elaborated by detailed thesis research, both in the field and in a systematic evaluation of results reported in the published literature.
BROADENING THE CONSIDERATION OF MICROBIAL SERVICES
Since 2001 when Andriankaja conducted his thesis research in Madagascar and when Professor Robert reported these findings at the SRI conference in China the next year, our understanding of how the life in the soil contributes to the effectiveness of SRI practices has expanded considerably. As discussed below, the contribution of microorganisms is not only in the soil but also within the rice plants themselves. Bacteria and fungi are both involved, as are also actinomycetes. The availability of both nitrogen and phosphorus, the two main building blocks for plant growth and reproduction, is increased by microbial activity, which is also associated with the mobilization and uptake of micronutrients.
Research in China has shown that the services of actinomycetes, a major phylum of bacteria, are also enhanced by SRI management practices. At the same time, other research in China showed a beneficial pattern when measurements were made of the nitrogen and carbon in the soil that was attributable to the microbial biomass there, relating these different levels to the effects on yield when rice was grown with SRI methods.
The first of the three figures shown below, from research by Limei Zhao for her PhD thesis at Zhejiang University, showed evident acceleration of tillering in SRI rice plants at about 25 days after they were transplanted. This has been widely seen by farmers and researchers in many countries, but how to explain what was going on? As seen in the other two figures from Limei’s research, at all stages of growth in the SRI plots compared to plots traditionally flooded (TF), there were higher levels of microbial biomass carbon (MBC), a standard measure of the amount of microbial life in the soil. The same was true also for microbial biomass nitrogen (MBN), which is the amount of nitrogen in the soil that comes from microbial sources.
In the traditional-flooding plots, the level of MBN was seen to be highest at the booting stage, when the rice plants’ begin to create grains, while in the SRI plots, the highest level of MBN was during the grain-filling stage, which most directly influences eventual crop yield. Note further that with SRI management, the MBN at grain-filling stage was 50% higher than the highest MBN recorded in TF plots at the preceding stage when grain formation was starting.
At harvest time, MBN levels in the SRI plots were more than 3x higher than measured in the TF plots. This research showed below-ground microbial dynamics and changes that contribute to the greater plant tillering seen in the first figure and then to 26% more grain yield in these trials.
As we learned more about the relationships between plants and microbes, the causal connections became more complicated. We mostly had to draw on research evaluating general plant-microbe relationships, not specifically influenced by SRI practices because systematic research on SRI was just getting started.
Research conducted in Egypt showed how rhizobia that inhabit the root nodules of clover, a legume, when grown in rotation with rice or wheat crops contributed to higher yield of these two grains, and not by fixing nitrogen. There were broader beneficial effects on the grain plants from these bacteria living in their root zones and in the plants themselves. Field studies showed some similar effects also with maize grown in the U.S.
One of the most interesting findings from this research in Egypt was the positive feedback between the growth of plants’ roots and the presence and services of beneficial bacteria, shown in the figures below. The presence of certain bacteria in the rhizosphere enhanced the growth of plants’ roots in multiple ways.
These figures showed the effect of inoculating two different varieties of rice with a particular microorganism (Rhizobacterium leguminosarum bv. trifolii 11) that inhabits nodules in clover roots in the study area but is also found around and in the roots of rice. Inoculation of young rice seedlings with these bacteria was found to affect – and greatly affect -- the architecture of the plants’ root systems in terms of their profusion (number of rootlets per plant), cumulative root length (in mm), surface area (cm²), and volume (cm³).
The Egyptian research reporting four different measurable effects of beneficial microbes on roots’ structure and size helped to make sense of the picture sent from Cuba, seen in Chapter 1, showing profuse SRI root growth. Luis Romero’s paddy soils when managed with SRI practices probably had an unusual abundance and activity of beneficial soil organisms that could stimulate so much root growth. Evidently more was involved in this profuse growth than just nutrient availability and uptake.
As we understood better the association between soil organisms and root growth, we could see that the root growth promotion stimulated by symbiotic microbes was not just altruistic. The mutualistic relationship between microorganisms and plant roots posed a significant question in evolutionary terms: how could this relationship have continued over several hundred million years if both parties did not each derive greater benefits from their association with each other than the respective costs that each had to bear within the relationship?
It has been calculated that up to 40% of the carbon that plants fix through photosynthesis in their leaves is exuded into the soil around their roots, along with a variety of amino acids, organic acids and other compounds that are metabolically synthesized in the plant and exuded through its roots. These exudates nourish and support the microbial populations that live around and on the roots to such an extent that such microorganisms are 10 to 100 times more abundant in the rhizosphere soil surrounding the roots like a glove than in the bulk soil beyond, which is not influenced by plants’ root exudation.
We have already noted many services that microbes provide to plants such as N fixation, P solubilization, nutrient mobilization and immobilization (conserving nutrients within the soil), protection against pathogens, induced systematic resistance to disease, etc. They also synthesize some of the same phytohormones that plants produce and need for their own growth.
If plants derived more benefit from the microbes that lived in, on and around them than the plants’ cost of producing so much and so many molecules that are exuded into the soil, this symbiotic relationship between plants and microbes could not have lasted for more than 400 million years. The ubiquity and productivity of this mutualistic relationship makes rather obsolete our tacit mental model of plants as carbon-based machines that we can design and redesign and manipulate simply for our purposes, without regard for their symbiotic microbial partners.
AN AMBITIOUS BOOK PROJECT ON THE LIFE IN THE SOIL
As both field observations, data and reading were sharpening my interest in soil biology, an unexpected event crystallized and deepened this interest. In April 2003, a senior editor of the Swiss scientific publishing house, Russell Dekker, came to my CIIFAD office at Cornell unexpectedly. From his base in New York City, he was visiting the university to make the rounds of persons who had previously published books with his firm, Marcel Dekker, soliciting ideas for new book projects.
When Russell Decker introduced himself, my first response was to thank him and his company for publishing a particular book on the rhizosphere that I had recently found very helpful and illuminating. This led into a discussion of SRI, to explain what had gotten me, a social scientist, interested in agricultural science. To convey to him that SRI ideas and impacts were not unique to Madagascar, I drew parallels between what I knew about SRI and what I had recently learned from a French agronomist, Olivier Husson, who was now working in Madagascar for the French international agricultural research agency CIRAD. Olivier had informed me about via email about some remarkable work experience in Vietnam.
Large areas within the Mekong Delta in Vietnam are classified as having acid sulphate soils with chemical, physical and biological properties that severely restrict their agricultural productivity. Olivier had told me about how a CIRAD project had undertaken a project to improve these soils considered inherently infertile. He and others working with him had found that these soils could be made productive by means similar to what we had employed in Ranomafana. They had modified crop establishment methods and water control, rather than rely on external chemical inputs. In Vietnam, innovations in soil management had brought 250,000 ha of this previously unproductive land into successful rice cultivation within about five years and at low cost.
After hearing my accounts from both Madagascar and Vietnam, Russell Dekker asked whether I would be interested in putting together a book on these kinds of approaches to raising agricultural production. He was not put off by my rather incredulous response (But I am a political scientist by training … ), saying that these innovative efforts deserved to be more widely known. He invited me to make a book proposal to his publishing house.
After a little reflection that afternoon, I called Erick Fernandes, the Cornell agronomist whose 1997 visit to Madagascar and encounter with SRI are described in Chapter 3. Erick had contributed to a previous book that I had edited on agroecological innovations. I assured him that I was willing to do most of the work on the proposed book, but I needed expert knowledge such as his on plant science, soil science and related subjects to be sure that the content was scientifically-sound. He had the expertise that I lacked to ensure that the book would have the requisite scientific rigor and merit. He agreed to join in the book project.
The next day, as it happened, I traveled again to Columbus, Ohio, to attend a conference on climate change and global food security at Ohio State University. Dr. Pedro Sanchez, an eminent soil scientist, and his wife Dr. Cheryl Palm, a noted tropical ecologist and soil microbiologist, were also participating. I asked both of them also to join in this book project since they worked on key aspects of the subject. Pedro had been Erick’s PhD professor at North Carolina State University, and having Erick already on board probably made the project more interesting to both Pedro and Cheryl. Again, I said that I would do most of the work required, but I needed to have their judgment on scientific matters. Within several months, an editorial team with both breadth and depth had been assembled.
This book project was like a multi-year post-doctoral fellowship, re-tooling a political scientist in soil science and crop science plus microbiology. The book was published in 2006 by CRC Press as Biological Approaches to Sustainable Soil Systems, with 102 contributors from 28 countries. Only one of the book’s 50 chapters was on SRI.
But the book’s core ideas stemmed from our SRI experience as expanded upon by Olivier’s experience in Vietnam, and then by many other congruent experiences and bodies of research that introduced me and others to subjects like phytohormones and biofertilization. M.S. Swaminathan, one of the most eminent agricultural scientists in the world and first recipient of the World Food Prize for his leadership in India’s Green Revolution (Chapter 21), wrote a supportive Foreword for the book.
A central theme of the book was that thinking and talking about ‘soil’ primarily in terms of its chemical and physical properties should be superseded by an appreciation of ‘soil systems’ that explicitly included and dealt with the soil’s biological dimensions. Soil systems are much more than their inert mineral components. They are made fertile by their biological elements, which extend from the uncountable, unseen organisms of the microbial realm up through the soil food web to visible creatures such as earthworms, ants and termites, all being essential to the functioning and productivity of soil systems. Previously the soil biota had been discussed in terms of a ‘soil food chain,’ but this metaphor was too linear. We preferred the idea of a ‘soil food web’ as conveying better the complexity and interactions involved than was implied by the word ‘chain.’
Despite the eminence, number and scope of its contributors, the book received little attention and response at the time, however. But its sales were good enough for the publisher, CRC Press, to suggest in December 2018, as this book on SRI was being put together, that the volume on soil systems be revised and updated for a second edition. Much had been learned in the dozen years since the first edition was published, especially about plant-microbial interactions and symbiosis. The analysis and conceptualization of the soil biology book were becoming more and more relevant.
More was learned about the role of microbes in SRI crop management from a three-year study supported by the World Wide Fund for Nature (WWF) and conducted jointly by the Directorate of Rice Research of the Indian Council for Agricultural Research (ICAR), the Andhra Pradesh state agricultural university (ANGRAU), and the International Crop Research Institute for the Semi-Arid Tropics (ICRISAT) (Chapter 8). That collaborative study included soil biology variables among many other parameters that were evaluated over four seasons, 2008 to 2010, assessing the effects of SRI management and comparing them with the practices being recommended by rice scientists.
Along with agronomic measurements like plant height, effective tillering, panicle length, shoot and root dry weight, and yield, the researchers evaluated microbial biomass nitrogen (MBN) and organic carbon (OC) in the soil, soil dehydrogenase (an enzyme that reflects the amount and activity of microbes in the soil), and total counts of bacteria, fungi, and actinomycetes. The conclusion from that long and thorough evaluation was: “SRI practices create favorable conditions for beneficial soil microbes to prosper, save irrigation water, and increase grain yield.” This summarized succinctly what we had been learning from diverse sources over the preceding decade.
BENEFICIAL MICROBES LIVE INSIDE PLANTS AS WELL AS ON THEM AND WITHIN THEIR ROOTS
Most of the research on the interdependence between plants and microorganisms has focused on plant root-microbial interactions below-ground, in the rhizosphere. In retrospect, I realize that our 2006 book had, regrettably, only five references to the phyllosphere, the domain above-ground where microorganisms live on plants’ leaves and other parts. When we started trying to understand SRI effects, little had been written about either phyllosphere organisms or about symbiotic endophytes, microbes that live within plants’ organs, in their tissues, and even within their cells.
Fortunately, the study of endophytes has become a burgeoning field of research for microbiologists. It turns out that Andriankaja’s research on symbiotic Azospirillum reported on at the start of this chapter was innovative and prescient thanks to Prof. Robert, as was the work reported above, done in Egypt by Youssef Yanni and Frank Dazzo with colleagues there.
Shortly after the soil biology book was sent off to the publisher, I received unexpectedly a paper on the effects of symbiotic endophytes in rice that reported the same kind of results as we were seeing and sometimes able to measure with SRI management. Feng Chi for his PhD degree in microbiology from the Institute of Botany in the China Academy of Sciences had done some paradigm-shifting work with five strains of rhizobia, published in a leading academic journal. It was too late to include this work in the book, but we struck up a long-distance acquaintanceship by email.
Chi had evaluated the effects of inoculating with five different strains of rhizobia the rice seedlings and soil in five sets of replicated 13-liter pots in which the seedlings had been planted. The pots were all filled with the same soil material, and the same rice variety was grown in all of them. Rice plants in a sixth set of pots that had no rhizobial inoculation were grown as controls for making comparisons.
The results, shown in the table below, were consistent and all statistically significant. Microscopic analysis using fluorescence-tagging techniques showed that the rhizobia in the soil after they entered into the plants’ roots then migrated up through the roots and shoots into the leaves, taking up residence throughout the plant.
All the rice plants that had been inoculated with rhizobia performed significantly better than the uninoculated control plants in all respects. They had significantly more root and shoot biomass, higher rates of photosynthesis and transpiration velocity, greater water utilization efficiency, and increased yield. They also accumulated significantly higher levels of growth-regulating hormones.
“Considered collectively, the results indicate that this endophytic plant-bacterium association is far more inclusive, invasive and dynamic than previously thought, including dissemination in both below-ground and above-ground tissues and enhancement of growth physiology by several microbial species.”
One could say that the plants had been ‘invaded’ or ‘infected’ by the microorganisms, but neither verb conveys quite the right sense. ‘Pervaded’ might be a better, more neutral word. Below are data from the article by Chi et al. which show the consistency of the effects significantly associated with soil bacteria inhabiting the interiors of the rice plants. Although these experiments were not conducted with SRI methods, we have seen all of these same effects when comparing SRI-managed rice plants with controls grown with standard methods.
The numbers in a column which have different letters are significantly different from the others with a statistical confidence level of 95%.
Five years later, Chi published further research on rice endophytes that used more advanced analytical methods. Proteomic analysis can identify which genes have caused significantly more (or less) synthesis of the particular proteins for which they are respectively responsible, in a molecular-biology process referred to as gene expression.
Chi’s experiments and measurements compared the gene expression of rice plants whose soil had been inoculated with Sinorhizobium meliloti 1021 (second row in the table above, Sm-1021) while they were still seedlings, grown from surface-sterilized seeds, with the proteins that had been synthesized in same-variety plants not inoculated and not containing this rhizobium. Sm-1021 had been the soil bacterium displaying the most potency in the previous research.
Microscopic examination confirmed that the rhizobia had entered the plants’ roots, and by 21 days after inoculation they had colonized the plants’ interior organs, their root hairs, aerenchyma, inter- and intra-cellular spaces of the epidermis, cortex, and other tissues. On the 7ᵗʰ, 14ᵗʰ and 21ˢᵗ days of growth, respectively, tissues from the rice plants’ roots, their leaf sheaths, and leaves were excised and examined. This was to ascertain whether there were any significant differences in the levels of specific proteins found in the tissues (significance being attributed to any increase or decrease that was greater than 50%). This analysis determined whether (and which) identifiable genes in the plant’s DNA had been up-regulated (or down-regulated) to synthesize more (or less) of the particular protein molecules being assayed.
The differences in gene expression between the inoculated and uninoculated rice plant tissues were very evident. Proteins in nine different functional categories were identified as being either up-regulated or down-regulated. A number of proteins related to photosynthesis were up-regulated in the leaf sheaths and leaves, for example, while defense-related proteins were more often up-regulated in the roots, although some defense mechanisms were also evoked in the above-ground tissues.
The figure below shows the relative frequency (in percent) with which the functioning of different kinds of genes was significantly up-regulated or down-regulated by the presence (versus absence) of the soil bacterium (Sm-1021) in the rice plants, grouped according to categories. In the root, sheath and leaf tissues, 31 genes were identified as up-regulated, mostly growth-promoting or for helping to defend against predators and disease, while 21 were down-regulated, some of the latter being genes that inhibit or regulate growth.
These microbially-induced changes in gene expression affected plant performance as seen from the fact that already at 14 days after inoculation, the inoculated plants had significantly greater root length (36%), more shoot height (7%), and increased shoot weight (44%). Among the genes up-regulated were those that govern the plant’s synthesis of growth hormones such as auxins which affect cell elongation in the rice plant shoot.
This particular organism, Sinorhizobium meliloti 1021, is known to be capable of fixing nitrogen, but its effects in this experiment were seen to involve the modification of plants’ gene expression. There was no direct connection with SRI management practices in this study, but the growth acceleration and the greater photosynthesis as well as the pest and disease resistance paralleled what was being seen in SRI-grown plants.
HOW SIMILAR EFFECTS ARE OBSERVED WITH BENEFICIAL FUNGI
These experimental results with bacterial endophytes became more interesting when we learned of similar effects with fungal endophytes, indeed with Fusarium culmorum, a fungal pathogen that is dreaded and despised by farmers for its causing blight and rot in wheat. This fungus demonstrated remarkable growth-stimulating effects in rice seedlings, according to research done by R.J. (Rusty) Rodriguez and colleagues.
Below is seen how different are the growth trajectories of rice plant roots when their sprouted seeds have been inoculated with Fusarium and then grown on a growth medium (agar) compared to the growth of uninoculated rice plant roots. In the four time-sequence pictures below, uninoculated plants are seen on the left, and the roots and shoots of inoculated plants are those on the right.
There was no visible difference when the plants were first placed on the agar (A); but after two days (B), there are evident differences in root length. By four days (C), the observable differences were even greater; and at eight days (D), the differences were not just in root length but also in the profuse branching of the roots of the inoculated plants.
At eight days one can already see differences in the above-ground growth. A difference that cannot be seen in the pictures is that root hairs, microscopic extensions of the root system which greatly expand its surface area, first emerged at three days after inoculation in the ‘infected’ plants, while it took five days for root hairs to begin emerging from the roots of rice seedlings that did not have the benefit of stimulus from this frequently pathogenic fungus.
Mechanisms for these effects are still being studied, but how symbiotic viruses confer resistance in grasses to the stresses of drought, salt and heat are being documented, and these effects, such as decrease in water consumption, were similar to what we were seeing with SRI management in rice. They reinforced a view that plants should not be regarded simply as organisms to be cajoled or coerced into producing more, but rather as conglomerates of plant and microbial cells that function in ways much more interdependent and complex than the image of plants that prevails within the public and among much although not all of the scientific community.
Working with some of the colleagues whose cutting-edge work is reviewed above, we prepared a chapter for the 2013 yearbook of CRC Press on ‘advances in soil science’ at the invitation of its eminent editor Dr. Rattan Lal. That chapter had little impact as far as we can tell, but it provided evidence of how agricultural productivity is shaped by the microbial realm. It also offered some avenues for explaining how SRI methods achieve the effects on plant growth and productivity that anyone could see. It further provided a basis for working with others on the beneficial impacts of endophytic bacteria and fungi, which are becoming better documented and appreciated.
MICROBES LIVING WITHIN PLANTS CELLS AFFECT PLANT GROWTH
In 2013, my wife Marguerite and I visited China for an agricultural conference in Hangzhou. While in Beijing, we made contact with Feng Chi’s mentor, Dr. Y.X. Jing, emeritus professor in the Institute of Botany within the China Academy of Sciences. Personal rapport was reinforced by learning that Jing and Frank Dazzo had both been post-doctoral fellows in microbiology together at the University of Wisconsin at Madison some 30 years earlier. Jing had spent a lifetime working in areas such as biological nitrogen fixation, and he had guided Feng Chi to study symbiotic microbes, first a set of rhizobial bacteria, and then specifically Sinorhizobium meliloti 1021.
Work on this organism had progressed from agronomic assessment in the 2005 article on the effects of inoculating rice plants with this bacterium, to proteomic analysis in the 2010 article. As discussed above, proteomics enabled researchers to assess by a somewhat crude methodology which genes in the bacterial genome, each responsible for the cell’s synthesis of a particular protein, were being up-regulated or down-regulated by interaction with the endophytic microbial organisms, thereby affecting the plant’s structure and physiological processes.
From our conversation, Marguerite and I learned about current work that Jing and his colleagues in the Institute of Botany were engaged in. They were doing transcriptomic analysis of the effects that introducing the rhizobium Sm-1021 into rice plants under carefully controlled conditions had on the gene expression of the rice plant’s cells.
With next-generation gene sequencing that analyzed the messenger RNA in cells, one could identify which specific genes were significantly up- or down-regulated in rice plants that were inhabited by symbiotic microorganisms, compared to identically-grown plants that had been inoculated with dead Sm-1021 microbes rather than with live organisms. Using sophisticated equipment, the researchers could count, at any particular time, how many differentially-expressed genes (DEGs) there were in the cells, and more importantly, they could identify which genes had been up-regulated or down-regulated.
Microscopic examination showed that tissues and cells in the roots, stems and leaves of the inoculated plants were inhabited by live microorganisms. These had entered the roots from the soil and then migrated upward into the stems and leaves. By direct measurements they could determine that physical growth had been accelerated in the inoculated plants, compared to those not hosting Sm-1021. At 5 and 8 days after inoculation, the height and weight of the inoculated rice shoots were 30% greater than the shoots of the control plants. At the cellular level, they documented that the size and the shape of tissue cells in the inoculated plants were different from those in uninoculated plants.
Most interesting were the changing patterns of gene expression, with accelerated and then decelerating rates at which certain genes were up-regulated or down-regulated over time. On the first day after inoculation, there were 195 DEGs; then 1,390 DEGs on day 2, 1,025 DEGs on day 5, and 533 DEGs on day 8. From looking at which genes were up- or down-regulated, one could infer how the plant’s pattern of gene expression changed from initial resistance to an intruder, to a gene profile of more neighborly acceptance.
The DEGs that were elevated at 5 and 8 days after inoculation were ones that affect the plant’s production of phytohormones, its photosynthetic efficiency, its carbohydrate metabolism, cell division, and wall expansion. The profile of up-regulated DEGs corresponded with measurable differences in plant growth.
While this research had nothing directly to do with SRI, the changes in plant performance that it showed resembled those that are seen with SRI management. I was quick to agree when Jing invited me to help him and his colleagues in writing up this research, to help polish its English for publication, and to relate what they were showing experimentally to broader concerns for understanding plant-microbial interaction. They also invited Frank Dazzo at Michigan State University to join as a co-author and bring his insights to bear on these findings, particularly addressing the biochemical signaling that must be occurring within the rice plants to elicit the evident changes in molecular biology.
Beginning in 2014, I started working with an Indonesian PhD candidate in microbiology at the national university in Malaysia (UKM), Febri Doni, whom I met at the 4th International Rice Congress held in Bangkok. Febri had been assisting Malaysia’s national SRI network (SRI-Mas) as a volunteer, and we quickly became friends. Febri added me to his committee of thesis advisors as an external member, to oversee his research on the beneficial and ubiquitous soil fungus Trichoderma, assessing its symbiotic effects when used in conjunction with SRI crop management practices.
I had become interested in Trichoderma from the soil biology book project discussed above. The work of Rusty Rodriguez and his colleagues had made clear that fungi could benefit crop plants as symbiotic endophytes just as bacteria could. Febri’s research strengthened our understanding of the beneficial effects of symbiotic microbes when coupled with SRI practices. Indeed, it led to a published article reviewing ways in which microorganisms definitely were or could be hypothesized to be contributing to the SRI effects reported in this book.
When I shared with Febri the findings of research done by Feng Chi and Prof. Jing, he became quickly interested in doing transcriptomic analysis to illuminate what was happening at the level of molecular biology in rice plants being grown with SRI methods and Trichoderma inoculation, compared with plants having just one of these treatments, or having neither. The data from such analysis identified a number of genes that were significantly up-regulated by having both treatments, compared with only one or neither.
The figure below is from a presentation that Febri made at an international conference on agriculture and climate change in Barcelona, Spain, in March 2017. It lists specific genes that his analysis identified as being expressed more vigorously in rice plants grown with SRI methods and Trichoderma inoculation. This prompted him to start research at UKM to identify which if any genes are activated just by SRI management methods compared to standard rice-growing practices. The effects would probably be mediated by microbes, but that presented an even more complex problem of analysis.
This does not mean that there was no microbial contribution to the SRI plants’ performance in Febri’s trials. We have come to understand that the microbial realm makes major and multiple contributions to SRI success with and through the larger, better-functioning root systems that were discussed in the preceding chapter. Starting with Andriankaja’s research at Anjomakely in 2001, our interest in microorganisms, and specifically in the microbiome, has grown and diversified.
The main impact has been to understand that plants are not just plants. When we look at a rice plant, we should ask ourselves what is being done, for better or worse, by the plant-microbial interactions and interdependencies taking place? Our understanding of this is still in nascent stages. But the continuing efforts to explain SRI effects will take us more deeply into the microbial domain.
[THIS CHAPTER WILL BE EXTENDED BY THE RESULTS OF THE RESEARCH AT UKM WHEN THESE BECOME AVAILABLE AT THE END OF 2020]
NOTES AND REFERENCES
 Comprehensive but fairly technical reviews of plants’ microbiomes include T.R. Turner, E.K. James and P.S. Poole, ‘The plant microbiome,’ Genome Biology, 14:20 (2013); G. Berg, M. Grube, M. Schlother and K. Smalla, ‘The plant microbiome and its importance for plant and human health,’ Frontiers in Microbiology, https://doi:10.3389/fmicb 2014.00491 (2014); and K. Schlaeppi and D. Bulgarelli, ‘The plant microbiome at work,’ Molecular Plant-Microbe Interaction, 28: 212-217 (2015).
 C.M. Pieterse C. Zamioudis, R.L. Berendsen, D.M. Weller, S.C. Van Wees and P.A. Bakker, ‘Induced systemic resistance by beneficial microbes,’ Annual Review of Phytopathology, 52: 347-375 (2014). On phytohormones, see A. Khalid, M. Arshad and Z.A. Zahir, ‘Phytohormones: Microbial production and application,’ in N. Uphoff et al., eds, Biological Approaches to Sustainable Soil Systems, 207-220, CRC Press, Boca Raton, FL (2006).
 B. Reinhold-Hurek and T. Hurak, ‘Living inside plants: Bacterial endophytes,’ Current Opinion in Plant Biology, 14: 435-443 (2011); G. Santoyo, G. Moreno-Hagelsieb, C. Orozco-Mosqueda and B.R. Glick, ‘Plant growth-promoting bacterial endophytes,’ Microbiologial Research 183: 92-99 (2016); Gary Harman and N. Uphoff, ‘Symbiotic root-endophytic soil microbes improve crop productivity and provide environmental benefits,’ Scientifica (2019).
 Good preparation for this line of investigation was reading the book Microcosmos: Four Billion Years of Evolution from our Microbial Ancestors written by Lynn Margulis with her son Dorion Sagan (Yale University Press, 1986), with a paperback edition from the University of California Press (1997). I happened to pick up this book for airplane reading as I was first learning about SRI and consider it one of the ten books that everyone should read to become better prepared for life.
 S.K. DeDatta, one of the most senior agronomists at the International Rice Research Institute for many years, had written in his comprehensive book on rice growing, "The microbial flora causes a large number of biochemical changes in the soil that largely determine the fertility of the soil" (page 60, emphasis added). Principles and Practices of Rice Production, Wiley, New York (1981). This appreciation, however, was not expressed throughout the book.
 ‘Understanding the Functioning and Management of Soil Systems,’ in Biological Approaches to Sustainable Soil Systems, eds. N. Uphoff, A. Ball, E. Fernandes, H. Herren, O. Husson, M. Laing, C. Palm, J. Pretty, P. Sanchez, P. Sanginga and J. Thies, 3-13, CRC Press, Boca Raton, FL (2006).
 Kateryn Zhalnina et al., ‘Dynamic root exudate chemistry and microbial substrate preferences drive patterns in rhizosphere microbial community assembly,’ Nature Microbiology, 3:470-480 (2018).
 Limitations and Potentials for Biological Nitrogen Fixation in the Tropics, Springer, Boston MA (1978). See also R.M. Boddy and J. Döbereiner, ‘Nitrogen fixation associated with grasses and cereals: Recent progress and perspectives for the future,’ Fertilizer Research, 42: 241-250 (1995). Döbereiner, born and educated in Europe, spent four decades in Brazil doing path-breaking work on nitrogen-fixing bacteria in sugar and rice and trained a whole generation of researchers to carry on this effort.
 Elaine R. Ingham, ‘Soil fungi,’ on the USDA Natural Resources Conservation Service website.
 The most noted work on this is the book by S.E. Smith and D.J. Read, Mycorrhizal Symbiosis, 3rd ed., Academic Press, New York (2008). Recent research in the UK indicates that the transformation of our earth’s atmosphere from high CO2 concentrations to abundance of oxygen during the Paleozoic era (>500-250 million years ago) is attributable to the activity of mycorrhizal fungi which symbiotically inhabited the roots of primitive plants, i.e., we would not be here without them. B.J.W. Mills, S.A. Butterman and K.J. Field, ‘Nutrient acquisition by symbiotic fungi governs Paleozoic climate transition,’ Philosophical Transactions of the Royal Society B, 373 (2017).
 N.S. Bolan, ‘A critical review on the role of mycorrhizal fungi in the uptake of phosphorus in plants,’ Plant and Soil, 134: 189-207 (1990).
 ‘Diazotrophic’ means nitrogen-fixing. O. Steenhoudt and J. Vanderleyden, ‘Azospirillum, a free-living, nitrogen-fixing bacterium closely associated with grasses: Genetic, biology and ecological aspects, FEMS Microbiology Review, 24: 487-506 (2000).
 Why Azospirillum has beneficial effects on plants’ growth and health is not fully known; more is involved than just its nitrogen-fixing capability, but there are many positive effects, as discussed in Y. Bashan and L.E. de-Bashan, ‘How the plant-growth promoting bacterium Azospirillum promotes plant growth: A critical assessment,’ Advances in Agronomy, 108: 77-136 (2010).
 These results were reported in a thesis by Andry Andriankaja, Mise en evidence des opportunités de développement de la riziculture par adoption du SRI et evaluation de la fixation biologique de l'azote: Cas des rizieres des hautes terres, Memoire de fin d'etudes, Ecole Superieure des Sciences Agronomique, University of Antananarivo (2001). Andry, after getting a PhD in Europe, has become a project manager for BASF at its base in North Carolina, working in biotechnology on making canola oil healthier, by increasing its omega-3 fatty acid content.
 This effect is well-known. See literature cited and data in J. Zhou et al., ‘Consistent effects of nitrogen fertilizer on soil bacterial communities in black soils for two crop seasons in China,’ Scientific Reports, 7: 3267 (2017).
 Iswandi Anas, O.P. Rupela, T.M. Thiyagarajan and N. Uphoff, ‘A review of studies on SRI effects on beneficial organisms in rice soil rhizospheres,’ Paddy and Water Environment, 9: 53-64 (2011). The data are from a thesis by G. Gyathry, ‘Studies on dynamics of soil microbes in rice rhizosphere with water saving irrigation and in situ weed incorporation,’ Tamil Nadu Agricultural University, Coimbatore, Tamil Nadu, India (2002); O.P. Rupela et al., ‘Comparing soil properties of farmers’ fields growing rice by SRI and conventional methods,’ paper prepared for the 1st national SRI symposium, ANGRAU, Hyderabad, Nov. 17–18, Worldwide Fund for Nature-ICRISAT (2006); and Iswandi Anas, T. Hutabarat and B. Muchlis, ‘Populasi mikroba tanah pada system of rice intensification (SRI),’ unpublished manuscript, Soil Biotechology Laboratory, Department of Soil Sciences, Institut Pertanian Bogor, Bogor, Indonesia (2010).
 K.G. Cassman, S. Peng, D. C. Olk, J. K. Ladha, W. Reichardt, A. Dobermann and U. Singh, ‘Opportunities for increased nitrogen-use efficiency from improved resource management in irrigated rice systems,’ Field Crops Research, 25: 7-39 (1998).
 S.B. Sharma, R.Z. Sayeed, M.H. Trivedi and T.A. Gobi, ‘Phosphorus-solubilizing microbes: Sustainable approach for managing phosphorus deficiency in agricultural soils,’ Springerplus, 2:587 (2013).
 Benjamin L. Turner and Philip M. Haygarth, Nature, 411: 258 (17 May 2001).
 B.L. Turner, M.J. Papházy, P.M. Haygarth and I.D. McKelvie, ‘Inositol phosphates in the environment,’ Philosophical Transactions of the Royal Society, London, Series B, 357: 449-469 (2002), and other publications which followed. See also B.L. Turner, E. Frossard and A. Oberson, ‘Enhancing phosphorus availability in low-fertility soils,’ in N. Uphoff et al., eds., Biological Approaches to Sustainable Soil Systems, 191-205, CRC Press, Boca Raton, FL (2006), and A.E. Richardson and R.J Simpson, ‘Soil microorganisms mediating phosphorus availability: Update on microbial phosphorus, Plant Physiology, 156: 989-996 (2011).
 ‘Organic phosphate in Madagascan soils,’ Geoderma, 136: 279-288 (2006).
 Marie-Soleil Turmel, Benjamin Turner and Joanne Whalen, ‘Soil fertility and yield response to the System of Rice Intensification,’ Journal of Renewable Agriculture and Food Systems, 26: 185-192 (2011). This data base was almost twice as large as that in the previous meta-analysis of SRI results: A. McDonald, P. Hobbs and S. Riha, ‘Does the system of rice intensification outperform best management? A synopsis of the empirical record,’ Field Crops Research, 96: 31-36 (2006), and it did not arbitrarily exclude certain comparisons.
 Marie-Soleil Turmel, Soil Properties and the Response of Rice Production to Water Regime and Fertilizer Source in Low Fertility Soils in the Republic of Panama, Ph.D. thesis, Plant Science Department, McGill University, Montreal, Canada (2011).
 ‘Research results on biological nitrogen fixation with the System of Rice Intensification,’ in N. Uphoff et al., eds., Assessments of the System of Rice Intensification: Proceedings of an International Conference, Sanya, China, April 1-4, 2002, 148-157, CIIFAD, Ithaca, NY.
 A. Adak, R. Prasanna, S. Babu, N. Bidyarani, S. Verma, M. Pal., Y. S. Shivay, and L. Nain, ‘Micronutrient enrichment mediated by plant-microbe interactions and rice cultivation practices,’ Journal of Plant Nutrition, 39: 1216–1232 (2016).
 Lin Xianqing, Zhu Defeng and Lin Xinjun, ‘Effects of water management and organic fertilization with SRI crop practices on hybrid rice performance and rhizosphere dynamics,’ Paddy and Water Environment, 9: 33-39 (2011). This research examined the interactions among variations in fertilizer and nutrient management, on one hand, and actinomycete populations, on the other. The latter were taken as an indicator of the total number aerobic organisms in the soil. On actinomycetes generally, see A.A. Bhatt, S. Haq and R.A. Bhat, ‘Actinomycetes benefaction role in soil and plant health,’ Microbial Pathogenesis, 111: 455-467 (2017).
Actinomycetes are known to enhance soil fertility (when there are sufficient organic sources of nutrients in the soil) and to be antagonists against a wide range of soil and plant pathogens. In the experiments reported, dry matter and leaf area index were seen to increase with alternate irrigation in association with increases in organic fertilization, holding equal the total amounts of N provided. With alternate wetting and drying, going from 25% to 100% organic fertilization increased the numbers of actinomycetes by 292%, whereas under continuous flooding, making the same change in fertilization only raised their numbers by 78%.
 L.M. Zhao, L.H. Wu, Y.S. Li, S. Animesh, D.F. Zhu and N. Uphoff, ‘Comparisons of yield, water use efficiency, and soil microbial biomass as affected by the System of Rice Intensification,’ Communications in Soil Science and Plant Analysis, 41: 1-12 (2010). This research is an example of how fortuitous connections have contributed to the understanding of SRI. Dr. Wu, an environmental scientist at Zhejiang University concerned with soil-nitrogen relationships, spent several months as a visiting research fellow at Cornell University in 2006. By chance, we happened to get acquainted shortly before he returned to China.
Back at his university, given his interest in reducing the overuse of N which has adverse effects on China’s water and soil, Wu encouraged Ms. Zhao, a PhD student working with him, to undertake her thesis research on SRI. She published three articles from this research, including one in Experimental Agriculture on ‘Influence of the System of Rice Intensification on rice yield and nitrogen and water use efficiency with different N application rates,’ written with Wu, three other Chinese colleagues and myself as co-authors, 45: 275-286 (2009). The article discussed here helped to advance understanding of the contributions made by soil microbes.
 The evaluations were done at four critical stages in the life cycle of rice: the tillering stage of vegetative growth; the booting stage when grain formation begins with panicle initiation; the grain-filling stage; and finally, harvest.
 By sheer coincidence, I happened to get acquainted in 2001 with Frank Dazzo, a soil microbiologist at Michigan State University, who had worked on this research in the Nile delta with an Egyptian microbiology colleague Youssef Yanni. I had been invited to Michigan State to give a presentation on some of my previous social science work, introducing participatory irrigation management in Sri Lanka. After the lecture I went to a retirement event honoring a MSU professor and friend, Richard Harwood. There I happened to meet a Cornell alumnus teaching at Michigan State who introduced me to his colleague Frank Dazzo.
When I told Frank about Andriankaja’s findings on Azospirillum in Madagascar, reported above, he became interested in SRI because these results were similar to those from his own work with Yanni on rhizobacteria in cereal crops in Egypt. Together they contributed a chapter to a book that I subsequently put together and edited, which is discussed below: ‘The natural Rhizobacterium-cereal crop association as an example of plant-bacteria interaction,’ in N. Uphoff et al., Biological Approaches to Sustainable Soil Systems,’ 109-127, CRC Press, Boca Raton, FL (2006).
 Y.G. Yanni et al., ‘The beneficial plant growth-promoting association of Rhizobacterium leguminosarum bv. trifolii in rice roots,’ Australian Journal of Plant Physiology, 28: 845-870 (2001). There were 24 co-authors of this paper, including Frank Dazzo, James Hill and J.K. Ladha, the latter two being senior scientists at IRRI. A more recent study in Brazil reports similar effects: M.C.F. Rêgo, F. Ilkiu-Borges, M.C.C. de Filippi, L.A. Gonçalves and G.B. da Silva, ‘Morphoanatomical and biochemical changes in the roots of rice plants induced by plant growth-promoting microorganisms,’ Journal of Botany (2014). https://www.hindawi.com/journals/jb/2014/818797/
 J.M. Lynch and J.M. Whipps, ‘Substrate flow in the rhizosphere,’ Plant and Soil, 129: 1-10 (1990).
 Horst Marschner, Mineral Nutrition in Higher Plants, Academic Press, London (1995); T.S. Walker, H.P. Bais, E. Grotewold and J.M. Vivanco, ‘Root exudation and rhizosphere biology,’ Plant Physiology, 132: 44-51 (2003); D.V. Badri and J.M. Vivanco, ‘Regulation and function of root exudates,’ Plant, Cell and Environment, 32: 666-681 (2009).
An excellent summary on the rhizosphere has been written by Völker Romheld and Günter Neumann, ‘The rhizosphere: Contribution of the soil-root interface in sustainable soil systems,’ for my edited book, Biological Approaches to Sustainable Soil Systems,’ 91-107, CRC Press, Boca Raton, FL (2006). The more comprehensive discussion, from which I was first instructed about these relationships, was a book edited by R. Pinton at al., The Rhizosphere: Biochemical and Organic Substances at the Plant-Soil Interface, Marcel Dekker, New York (2001).
 S. Spaepen, ‘Plant hormones produced by microbes,’ in B. Lugtenberg, ed., Principles of Plant-Microbe Interaction, 247-256, Springer, Cham, Switzerland (2014).
 The Marcel Dekker publishing house was bought up by the UK-based publisher Taylor & Francis later in 2003.
 The previous year, I had helped co-edit the proceedings from a 2001 conference organized at Ohio State University by Rattan Lal on Sustainable Agriculture and the International Rice-Wheat System. This book, published by Marcel Dekker in 2004, qualified me for a visit from this publisher’s editor Russell Dekker as he had overseen that book project.
 This book on the rhizosphere is referenced at the end of endnote 32 above. Russell Dekker’s generous response to my thanking him for this book was to send me gratis the huge reference book on roots that is referred to in an endnote in Chapter 4. That book edited by Israeli scientists greatly expanded my knowledge on how roots do much more than just anchor plants in the soil and take up water and nutrients for them.
 This connection was one of the most remarkable in the SRI story. While I was director of CIIFAD, its interdisciplinary working group on Mulch-Based Agriculture supported an on-line discussion engaging persons interested in capitalizing upon biological dynamics in crop-soil systems. (The group’s discussions were facilitated by Lucy Fisher, who also started the SRI website and still manages it.) One member of the group, to be provocative, had posted a comment to the effect that he thought the only way to enhance the productivity of nutrient-poor tropical soils was by applying chemical fertilizer, rather than relying on mulch and other organic media.
This elicited a lot of internet controversy, and Lucy suggested that I contribute something on the experience of SRI in Madagascar, where we had seen a quadrupling of rice yields from starkly-deficient soils under SRI management relying just on organic inputs as discussed in Chapter 3. She thought this would add substance to the discussion. A few days after posting an account of our SRI experience, I got a long email response from Olivier Husson, who had somehow gotten my posting through a friend of a friend. Olivier’sl email told me that he had had very similar experience in Vietnam, remedying low-productivity ‘problem’ soils just by making changes in their management rather than by applying external inputs.
 This has been written up by Olivier Husson with Lucien Séguy, Roger Michellon, and Stéphane Boulakia, ‘Restoration of acid soil systems through agroecological management,’ in N. Uphoff et al., Biological Approaches to Sustainable Soil Systems,’ 343-356, CRC Press, Boca Raton, FL (2006).
 Agroecological Innovations: Increasing Food Production with Participatory Development, Earthscan, London (2002). This book presented papers from a 1999 conference held on this subject at the Rockefeller Foundation center in Bellagio, Italy, my first venture into this area.
 Sanchez’s book on Properties and Management of Soils in the Tropics, first published in 1976 by John Wiley, New York, and republished in 2019 by Cambridge University Press, has been a classic on this subject for 40 years. In 1972, while serving as co-leader of a national rice program in Peru, Pedro had published an article with N. Larrea on ‘Influence of seedling age at transplanting on rice performance,’ Agronomy Journal 64: 828-833. This documented the adverse effects of the delayed transplanting of seedlings, so he was already acquainted with some SRI issues. Pedro served as Director-General of the Centre for International Agroforestry Research (CIFOR) from 1991 to 2001 and was the World Food Prize laureate in 2002. As noted in Part II, in1998 he had invited me to give a seminar at ICRAF on our work in Madagascar. This was the second public presentation that I made on SRI. His wife Cheryl was a principal research scientist with the CGIAR’s Tropical Soil Biology and Fertility (TSBF) program based in Kenya, and then senior research scientist at the Earth Institute at Columbia University. Both are now at the University of Florida.
 The editorial team included, in addition to Fernandes, Palm and Sanchez, two soil microbiologists (N. Sanginga, director-general of the Tropical Soil Biology and Fertility program, based in Kenya; and Janice Thies, professor of Crop and Soil Sciences at Cornell and faculty leader of CIIFAD’s Soil Health Working Group), an environmental microbiologist (Andy Ball, at the time director of the Centre for Environment and Society at the University of Essex in UK, and now Distinguished Professor at the Royal Melbourne Institute of Technology in Australia), an agronomist-ecologist (Olivier Husson, senior researcher with CIRAD, the French institute for international agricultural research), a biologist-environmentalist (Jules Pretty, Professor of Environment and Society at the University of Essex in UK), an entomologist-ecologist (Hans Herren, former director-general of the International Centre for Insect Physiology and Ecology in Kenya; president of the Millennium Institute in Washington, DC; and a World Food Prize laureate), and a plant pathologist who works on biological control, soil fertilization, and plant breeding (Mark Laing, director of the African Centre for Crop Improvement at the University of KwaZulu-Natal in South Africa), a diverse and eminent group.
 Robert Randriamiharisoa, Joeli Barison and N. Uphoff, ‘Soil biological contributions to the System of Rice Intensification,’ in N. Uphoff et al., Biological Approaches to Sustainable Soil Systems,’ 409-425, CRC Press, Boca Raton, FL (2006).
 See, for example, chapters contributed from Pakistan and from Cuba: A. Khalid, M. Arshad and Z.A. Zahir on phytohormones referred to above in endnote; and R.M. Viera and B.D. Alvarez, ‘Practical applications of bacterial biofertilizers and biostimulators,’ in N. Uphoff et al., Biological Approaches to Sustainable Soil Systems,’ 207-220 and 467-478, CRC Press, Boca Raton, FL (2006).
 Dr. Swaminathan had already done his own evaluations of SRI at his research foundation in India, as discussed in Chapter 20. In his Foreword to this book, he included an unsolicited endorsement of SRI: “Experience in India has shown that this methodology leads to nearly 40% saving in water without affecting the yield of the crop, indeed, as a rule, increasing crop yields with reduced external inputs.” (page iv)
 A really instructive, readable elaboration on this perspective is Tales from the Underground: A Natural History of the Subterranean World (Perseus, Cambridge, MA, 2001). Its author, David Wolfe, was one of the contributors to our volume.
 The soil food web was discussed in the volume by Thies and Grossman in ‘The soil habitat and soil ecology,’ pages, 59-78. A more extended discussion of this is provided by J.K. Whalen and L. Sampedro in their book Soil Ecology and Management (CABI Publishers, Wallingford, UK, 2010).
 Although the book was published and promoted by a major publishing house, the only journal that appears to have reviewed it, according to a Google search, was Landscape Ecology. Crop and soil scientists took little evident interest in this paradigm shift despite the number and stature of the volume’s contributors, although a number of professors used the book in their courses.
 In December 2018, the agriculture and nutrition editor of CRC Press asked if we would revise and update the book for a 2nd edition to be published in 2020. Practically all of the previous co-editors and contributors (who were still alive) readily agreed to this project, with the new edition slightly renamed: Biological Approaches to Regenerative and Resilient Soil Systems.
 ‘Assessment of different methods of rice (Oryza sativa L.) cultivation affecting growth parameters, soil chemical, biological, and microbiological properties, water saving, and grain yield in rice–rice system,’ by S. Gopalakrishnan, R. Mahender Kumar, P. Humayun, V. Srinivas, B. Ratna Kumari, R. Vijayabharathi, A. Singh, K. Surekha, Ch. Padmavathi, N. Somashekar, P. Raghuveer Rao, P. C. Latha, L.V. Subba Rao, V.R. Babu, B.C. Viraktamath, V. Vinod Goud, N. Loganandhan, B. Gujja and O.P. Rupela, Paddy and Water Environment, 12: 79-87 (2014).
 In reading a recent review article on plant endophytes, I found that three-quarters of the 100+ references in the bibliography had been published after our book on biological approaches to sustainable soil systems had been published. Z.A. Wani, N. Ashraf, T. Mohiuddin and S. Riyaz-Ul-Hassan, ‘Plant-endophyte symbiosis: An ecological perspective,’ Applied Microbiology and Biotechnology, 99:2955-2965 (2015).
 Chi wrote in November 2005 to a colleague in the Government Department at Cornell, Prof. Ron Herring, inquiring whether there would be any opening at Cornell for a post-doctoral fellowship in his research area. He attached his article, ‘Ascending migration of endophytic bacteria, from roots to leaves, inside rice plants and assessment of benefits to rice growth physiology, Applied and Environmental Microbiology, 71: 7271-7278 (2005), written with S.H. Shen, H.P. Chang, Y.X. Jing, Y.G. Yanni and F.B. Dazzo.
Ron forwarded the email and article to me because he, as a political scientist, did not work with either rice or microbes, and he knew that I was interested in both. It was stunning that two of Chi’s co-authors, Yanni and Dazzo, had contributed a chapter on plant-microbial interactions for the soil biology book discussed above (their chapter is cited in endnote 29). It is, indeed, a small world.
 Details of the experiment are given in the article by Chi et al. in preceding endnote.
 A.K. Thakur, N. Uphoff and E. Antony, ‘“An assessment of physiological effects of the System of Rice Intensification (SRI) compared with recommended rice cultivation practices in India,’ Experimental Agriculture, 46: 77-98 (2010).
 Details are given in Feng Chi, P.F. Yang, F. Han, Y.X. Jing and S.H. Shen, ‘Proteomic analysis of rice seedlings infected by Sinorhizobium meliloti 1021,’ Proteomics, 10: 1861-1874 (2010).
 Rodriguez, a microbiologist formerly working with the U.S. Geological Survey, and a network of colleagues in different institutions had found that fungal endophytes were affecting plant species’ reproductive success and resilience to environmental stresses, so their experiments with rice, summarized below, had little to do with their main professional work. But to test for growth-promotion effects, they had done trials with rice seedlings which were published in the Journal of Communicative and Integrative Biology by R.J. Rodriguez, D.C. Freeman, E.D. McArthur, Y.O. Kim and R.S. Redman, ‘Symbiotic regulation of plant growth, development and reproduction,’ 2:3, 1-3 (2009).
I only learned about this research because Roy Steiner, a former student of mine and co-author of a book on irrigation management, working on the agricultural staff of the Bill and Melinda Gates Foundation sent it to me, knowing of my interest in plant-microbial interaction. Rodriguez, having found government service too constraining for his innovative work with beneficial microorganisms, resigned from the USGS in 2012 to form a company that seeks to promote sustainable agriculture through utilization of microbial capabilities. The company’s current name is Adaptive Symbiotic Technologies. Rodriguez’s initiatives with fungal endophytes have been reported approvingly in Nature, ‘Food fueled with fungi,’ 504 (5479): 199 (2015).
 E.g., R.J. Rodriguez, J. Henson, E. Van Volkenburg, M. Hoy, L. Wright, F. Beckwith, Y.O. Kim and R. S. Redman, ‘Stress tolerance in plants via habitat-adapted symbiosis,’ ISME Journal, 2: 404-416 (2008).
 N. Uphoff, F. Chi, F.B. Dazzo and R.J. Rodriguez, ‘Soil fertility as a contingent rather than inherent characteristic: Considering the contributions of crop-symbiotic soil microbiota,’ in R. Lal and B. Stewart, eds., Principles of Sustainable Soil Management in Agroecosystems, 41-166, CRC Press, Boca Raton, FL (2013).
 A Cornell plant pathologist at the research station in Geneva, NY, Gary Narman, who has been in the forefront of research on the beneficial fungus Trichoderma, in 2018 invited me to co-author with him a review article, ‘Symbiotic root-endophytic soil microbes improve crop productivity and provide environmental benefits,’ published in Scientifica, 9106395 (2019).
 This was one of the earlier rhizobia to have its genome mapped: R.J. Honeycutt, M. McClelland and B.W. Sobral, ‘Physical map of the genome of Rhizobium meliloti 1021,’ Journal of Bacteriology, 175: 6945-6952 (1993). It is known to emit a rhizosphere-signaling molecule (lumichrome) that has been shown to promote the growth of soyabean, cowpea and maize, affecting root respiration, stomatal conductance, leaf transpiration, and the rate of photosynthesis. It has a photoreceptor that detects light and regulates various aspects of plant growth and development, including seed germination, stem elongation and leaf expansion. Curiously, as of 2018, the Wikipedia entry for this particular bacterium still made reference only to its plant-supportive role in the nodules of leguminous plants. It made no mention of the bacterium as a symbiotic endophyte in non-leguminous plants.
 Seedlings were grown from the surface-sterilized seeds of the same variety of rice, under conditions where other organisms had been eliminated as much as possible and the soil growth medium was managed so that the only biological/experimental variable was the presence or absence of Sm-1021. At 1, 2, 5 and 8 days after the soil had been inoculated with this bacterium, samples of seedling root and shoot tissues were taken. The respective cells were examined through microscopy, and their gene expression was tallied with a DNA-chip analyzer and microarray software. The methods are very advanced, although apparently rather routine for people studying molecular biology. With no training in this subject, I could never hope to fully understand the intricacies and have to rely on others more expert on these methods than I am.
 The article, ‘Rhizobia promote the growth of rice shoots by elevated cell signaling, division and expansion,’ by Q.Q. Wu, X.J. Peng, M.F. Yang, W.P., F.B. Dazzo, N. Uphoff, Y.X. Jing, and S.H. Shen, has been published in Plant Molecular Biology, 97: 507-523 (2018).
 Mark Laing, at the University of KwaZulu in South Africa, contributed a chapter on Trichoderma to the book and served as a co-editor: B. Neumann and M. Laing, ‘Trichoderma: An ally in the quest for soil system sustainability,’ in N. Uphoff et al., Biological Approaches to Sustainable Soil Systems, 491-500, CRC Press, Boca Raton, FL (2006). I was also interested in Trichoderma through the highly-regarded work of my Cornell colleague, Gary Harman. Like Rusty Rodriguez, Gary had found academic institutions to be very slow-moving and not very responsive to new knowledge and opportunities, so he had left academia to work with a private firm Advanced Biological Marketing.
 Febri, grasping the power and potentials of this beneficial soil organism, published two articles on Trichoderma and SRI before he had finished his thesis and had submitted a third for publication, all written with his advisors as co-authors: ‘Relationships observed between Trichoderma inoculation and characteristics of rice grown under System of Rice Intensification (SRI) vs. conventional methods of cultivation,’ Symbiosis, 72: 45-59 (2017); ‘A simple, efficient, and farmer-friendly Trichoderma-based biofertilizer evaluated with the SRI rice management system,’ Organic Agriculture, XX (2017); ‘Synergistic effects of System of Rice Intensification (SRI) management and Trichoderma asperellum SL2 increase the resistance of rice plants (Oryza sativa L.) against sheath blight (Rhizoctonia solani) infection,’ manuscript under review.
 F. Doni, M.S. Mispan, N.S.M. Suhaimi, N. Ishak and N. Uphoff, ‘Roles of microbes in supporting sustainable rice production using the System of Rice Intensification,’ Applied Microbiology and Biotechnology 103: 5153-5142 (2019).
 F. Doni, N. Uphoff, C.M.Z.C. Radziah, A. Isahak, F. Fathurrahman and W.Y. Wan Mohtar, ‘Physiological effects and transcriptomic profiling of rice plant-microbe interactions in a System of Rice Intensification (SRI) agroecosystem: Identifying phenotypical modifications to deal with climate change,’ presentation at the 2ⁿᵈ International Conference on Agriculture and Climate Change, March 26-28, 2017, Barcelona, Spain.
PICTURE CREDITS: Journal of Communicative and Integrative Biology, cited in endnote 55.