NSF Project - Summary

Chickpea and its wild relatives have a natural capacity for nitrogen fixation, reducing their dependence on exogenous nitrogen. Nevertheless domesticated legumes, including chickpea, often suffer from low and/or variable rates of nitrogen fixation (Kiers et al 2007, Brockwell et al., 1991; Schwenke et al., 1998; Herridge et al., 2005; Zahran, 1999; Rao et al., 2002). Multiple factors underlie this situation, including host genetics, the quality of applied and endemic rhizobia, as well as local edaphic and environmental influences. Initial data from our team suggests that shifts in the genetics of domesticated chickpea may have created legume crops that are more reliant on soil nitrogen and likely less able to harness symbiotic nitrogen fixation. Developing a detailed understanding of the genes that underlie these genetic shifts and deducing their evolutionary history and functional consequences are the primary focuses of this project. In the course of this research we expect to reveal novel aspects of the symbiosis. Doing so requires characterizing evolutionary outcomes in both natural and human-built environments, which we achieve by combining the traditionally separate domains of ecology and molecular biology, with genomics and quantitative biology serving as the bridge.

We hypothesize that a range of distinct genetic processes during domestication and recent breeding underlie altered nitrogen responses in chickpea. Among factors that might reduce function are selection trade-offs, selection relaxation, and random demographic processes (e.g., drift). A corollary to this logic is that natural populations of chickpea’s progenitor species, Cicer reticulatum, possess nitrogen fixation traits that are maintained by positive selection. These statements frame the major challenges and opportunities of this project, namely the need to deduce diverse selection histories in the context of natural and human-built environments, and to translate this information into candidate gene identification and stringent tests of gene function.

As important as single genotypes of model systems and forward genetics have been (and continue to be) for gene discovery, they are typically insufficient to inform us about the nature of standing genetic variation from which natural and human selection reshape organismal function. Bridging ecology and molecular biology by means of genomics and quantitative biology will permit identification and subsequent analysis of these evolutionarily active genes. We anticipate that the outcomes will include genes whose functions have not been identified in forward genetic screens. We anticipate describing the molecular genetic basis of long-standing, but poorly understood observations and questions. Is there a genetic basis for the often low and variable rates of nitrogen fixation in legume crops (Brockwell et al., 1991; Schwenke et al., 1998; Herridge et al., 2005; Zahran, 1999; Rao et al., 2002)? If so, has domestication contributed to this situation? To what extent does coevolution of plant and microbial populations contribute to efficient symbiosis across environments? What are the underlying genes, and are the “solutions” idiosyncratic or common to different populations? Do such solutions include novel alleles of well-described signaling proteins? Have such interactions been altered during domestication, and are the alterations adaptive or mal-adaptive?

The specific objectives of this study are:

1. To characterize the functional significance of standing variation in wild populations of Cicer reticulatum and its co-occurring bacterial symbionts, using ecology, genomics, and phenotyping.

2. To identify genomic footprints of domestication-associated shifts in genetic/genomic variation.

3. To identify the genes that underlie domestication-related shifts in nodule number and responsiveness to soil nitrogen, as well as of selected phenotypes and pathways discovered in Objectives 1 and 2.