skip to main content

Title: The Impacts of Domestication and Breeding on Nitrogen Fixation Symbiosis in Legumes
Legumes are the second most important family of crop plants. One defining feature of legumes is their unique ability to establish a nitrogen-fixing root nodule symbiosis with soil bacteria known as rhizobia. Since domestication from their wild relatives, crop legumes have been under intensive breeding to improve yield and other agronomic traits but with little attention paid to the belowground symbiosis traits. Theoretical models predict that domestication and breeding processes, coupled with high‐input agricultural practices, might have reduced the capacity of crop legumes to achieve their full potential of nitrogen fixation symbiosis. Testing this prediction requires characterizing symbiosis traits in wild and breeding populations under both natural and cultivated environments using genetic, genomic, and ecological approaches. However, very few experimental studies have been dedicated to this area of research. Here, we review how legumes regulate their interactions with soil rhizobia and how domestication, breeding and agricultural practices might have affected nodulation capacity, nitrogen fixation efficiency, and the composition and function of rhizobial community. We also provide a perspective on how to improve legume-rhizobial symbiosis in sustainable agricultural systems.
Authors:
; ; ; ;
Award ID(s):
1758037
Publication Date:
NSF-PAR ID:
10181524
Journal Name:
Frontiers in genetics
ISSN:
1664-8021
Sponsoring Org:
National Science Foundation
More Like this
  1. Global climate change and local anthropogenic activities are increasing soil salinization with permanent negative effects on agricultural and ecosystem productivity. While salt stress is known to affect plant performance, its effects on the association with key microbial plant symbionts, such as legume-associated nitrogen-fixing rhizobia, are less understood. In this field study conducted in Costa Rica (Puntarenas), we used sympatrically-occurring wild lima bean (Phaseolus lunatus L.) and Bradyrhizobium to quantify biomass production of unfertilized rhizobial (R+) and fertilized rhizobia-free (R-) plants at different levels of experimentally manipulated salinity in native soil. In response to salt stress, nodulation was significantly reduced evenmore »at slightly increased salt levels. Plants growing at soil salinity levels of 2, 4, 6, and 8 mS/cm showed a mean reduction of nodules by 60.22, 76.52, 83.98, and 92.5% compared to the controls. Similarly, we also observed a significant decline in plant biomass at elevated salinity. However, biomass accumulation of R- plants was significantly less impacted compared to R+ plants, suggesting that the plant-microbe symbiosis is more salt-sensitive than the plant host itself. We suggest that the search for more salt-tolerant, crop plant-compatible rhizobial strains may provide a sustainable approach to maintain agricultural productivity on low to moderately saline soils.« less
  2. Glass, Jennifer B. (Ed.)
    ABSTRACT The environmental context of the nitrogen-fixing mutualism between leguminous plants and rhizobial bacteria varies over space and time. Variation in resource availability, population density, and composition likely affect the ecology and evolution of rhizobia and their symbiotic interactions with hosts. We examined how host genotype, nitrogen addition, rhizobial density, and community complexity affected selection on 68 rhizobial strains in the Sinorhizobium meliloti – Medicago truncatula mutualism. As expected, host genotype had a substantial effect on the size, number, and strain composition of root nodules (the symbiotic organ). The understudied environmental variable of rhizobial density had a stronger effect onmore »nodule strain frequency than the addition of low nitrogen levels. Higher inoculum density resulted in a nodule community that was less diverse and more beneficial but only in the context of the more selective host genotype. Higher density resulted in more diverse and less beneficial nodule communities with the less selective host. Density effects on strain composition deserve additional scrutiny as they can create feedback between ecological and evolutionary processes. Finally, we found that relative strain rankings were stable across increasing community complexity (2, 3, 8, or 68 strains). This unexpected result suggests that higher-order interactions between strains are rare in the context of nodule formation and development. Our work highlights the importance of examining mechanisms of density-dependent strain fitness and developing theoretical predictions that incorporate density dependence. Furthermore, our results have translational relevance for overcoming establishment barriers in bioinoculants and motivating breeding programs that maintain beneficial plant-microbe interactions across diverse agroecological contexts. IMPORTANCE Legume crops establish beneficial associations with rhizobial bacteria that perform biological nitrogen fixation, providing nitrogen to plants without the economic and greenhouse gas emission costs of chemical nitrogen inputs. Here, we examine the influence of three environmental factors that vary in agricultural fields on strain relative fitness in nodules. In addition to manipulating nitrogen, we also use two biotic variables that have rarely been examined: the rhizobial community's density and complexity. Taken together, our results suggest that (i) breeding legume varieties that select beneficial strains despite environmental variation is possible, (ii) changes in rhizobial population densities that occur routinely in agricultural fields could drive evolutionary changes in rhizobial populations, and (iii) the lack of higher-order interactions between strains will allow the high-throughput assessments of rhizobia winners and losers during plant interactions.« less
  3. Stabb, Eric V. (Ed.)
    ABSTRACT Some soil bacteria, called rhizobia, can interact symbiotically with legumes, in which they form nodules on the plant roots, where they can reduce atmospheric dinitrogen to ammonia, a form of nitrogen that can be used by growing plants. Rhizobium-plant combinations can differ in how successful this symbiosis is: for example, Sinorhizobium meliloti Rm1021 forms a relatively ineffective symbiosis with Medicago truncatula Jemalong A17, but Sinorhizobium medicae WSM419 is able to support more vigorous plant growth. Using proteomic data from free-living and symbiotic S. medicae WSM419, we previously identified a subset of proteins that were not closely related to anymore »S. meliloti Rm1021 proteins and speculated that adding one or more of these proteins to S. meliloti Rm1021 would increase its effectiveness on M. truncatula A17. Three genes, Smed_3503, Smed_5985, and Smed_6456, were cloned into S. meliloti Rm1021 downstream of the E. coli lacZ promoter. Strains with these genes increased nodulation and improved plant growth, individually and in combination with one another. Smed_3503, renamed iseA ( i ncreased s ymbiotic e ffectiveness), had the largest impact, increasing M. truncatula biomass by 61%. iseA homologs were present in all currently sequenced S. medicae strains but were infrequent in other Sinorhizobium isolates. Rhizobium leguminosarum bv. viciae 3841 containing iseA led to more nodules on pea and lentil. Split-root experiments with M. truncatula A17 indicated that S. meliloti Rm1021 carrying the S. medicae iseA is less sensitive to plant-induced resistance to rhizobial infection, suggesting an interaction with the plant’s regulation of nodule formation. IMPORTANCE Legume symbiosis with rhizobia is highly specific. Rhizobia that can nodulate and fix nitrogen on one legume species are often unable to associate with a different species. The interaction can be more subtle. Symbiotically enhanced growth of the host plant can differ substantially when nodules are formed by different rhizobial isolates of a species, much like disease severity can differ when conspecific isolates of pathogenic bacteria infect different cultivars. Much is known about bacterial genes essential for a productive symbiosis, but less is understood about genes that marginally improve performance. We used a proteomic strategy to identify Sinorhizobium genes that contribute to plant growth differences that are seen when two different strains nodulate M. truncatula A17. These genes could also alter the symbiosis between R. leguminosarum bv. viciae 3841 and pea or lentil, suggesting that this approach identifies new genes that may more generally contribute to symbiotic productivity.« less
  4. Abstract Background For well over a century, rhizobia have been recognized as effective biofertilizer options for legume crops. This has led to the widespread use of rhizobial inoculants in agricultural systems, but a recurring issue has emerged: applied rhizobia struggle to provide growth benefits to legume crops. This has largely been attributed to the presence of soil rhizobia and has been termed the ‘rhizobial competition problem.’ Scope Microbiome engineering has emerged as a methodology to circumvent the rhizobial competition problem by creating legume microbiomes that do not require exogenous rhizobia. However, we highlight an alternative implementation of microbiome engineering thatmore »focuses on untangling the complexities of the symbiosis that contribute to the rhizobial competition problem. We outline three approaches that use different starting inocula to test hypotheses to overcome the rhizobial competition problem. Conclusions The approaches we suggest are targeted at various stages of the legume-rhizobium symbiosis and will help us uncover underlying molecular mechanisms that contribute to the rhizobial competition problem. We conclude with an integrative perspective of these different approaches and suggest a path forward for future research on legumes and their complex microbiome.« less
  5. Nitrogen (N) is an essential but generally limiting nutrient for biological systems. Development of the Haber-Bosch industrial process for ammonia synthesis helped to relieve N limitation of agricultural production, fueling the Green Revolution and reducing hunger. However, the massive use of industrial N fertilizer has doubled the N moving through the global N cycle with dramatic environmental consequences that threaten planetary health. Thus, there is an urgent need to reduce losses of reactive N from agriculture, while ensuring sufficient N inputs for food security. Here we review current knowledge related to N use efficiency (NUE) in agriculture and identify researchmore »opportunities in the areas of agronomy, plant breeding, biological N fixation (BNF), soil N cycling, and modeling to achieve responsible, sustainable use of N in agriculture. Amongst these opportunities, improved agricultural practices that synchronize crop N demand with soil N availability are low-hanging fruit. Crop breeding that targets root and shoot physiological processes will likely increase N uptake and utilization of soil N, while breeding for BNF effectiveness in legumes will enhance overall system NUE. Likewise, engineering of novel N-fixing symbioses in non-legumes could reduce the need for chemical fertilizers in agroecosystems but is a much longer-term goal. The use of simulation modeling to conceptualize the complex, interwoven processes that affect agroecosystem NUE, along with multi-objective optimization, will also accelerate NUE gains.« less