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Impacts of domestication on the rhizobial mutualism of five legumes across a gradient of nitrogen-fertilisation

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Abstract

Aims

Domestication and crop breeding has improved plants for human use, but may have unintended consequences for traits that are not selected upon. Disruption in the mycorrhizal mutualism has been observed in crops; possibly due to breeding in fertilised soil. Little is known about whether the legume-rhizobia mutualism can be disrupted by domestication and crop evolution, despite the importance of symbiotic nitrogen fixation. We aimed to identify differences in mutualistic outcomes between five legume cultivars and their wild progenitors in terms of their reactions across varying nitrogen levels.

Methods

With five greenhouse experiments, we characterised symbiosis traits in chickpea, lentil, pea, peanut, and soybean across a gradient of N fertilisation to characterise whether symbiosis traits differ context specifically between wild and domesticated lines.

Results

At lower levels of N addition, wild soybean benefited more from rhizobia than domesticated soybean. Chickpea cultivars abandoned symbiosis at lower N than wild chickpea accessions. Chickpea cultivars reduced per-nodule colony forming units (CFU) in response to N addition more than wild chickpeas, but lentil cultivars reduced CFU less than lentil accessions. The lentil, pea, and peanut cultivars did not differ from their wild relatives in rhizobial benefit, nor in nodulation response to N addition.

Conclusions

Differences in the regulation of the root nodule symbiosis are evident between domesticated and wild chickpea and soybean, but not lentil, pea, or peanut. This indicates that mutualism disruption—a decrease in the magnitude of the mutually symbiotic interaction—is a possible, but not necessary, consequence of domestication.

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Data availability

The data presented in this manuscript will be archived with Dryad upon acceptance.

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Acknowledgements

We thank those who provided germplasm: soybean cultivar MN1312CN (Aaron Lorenz, Department of Agronomy and Plant Genetics, University of Minnesota), peanut cultivars GA06G and Jupiter (Ricky Hartley, Golden Peanut Company and Jill Manahan, Oklahoma Foundation State Seed Stocks, respectively), pea cultivar Serge and lentil cultivar Pardina (Lyndon Porter, USDA), chickpea cultivar Sawyer and the lentil cultivar Avondale (Clarice Coyne, USDA), chickpea cultivar Sierra (Tiffany Fields, USDA), and wild peanut seeds (Shyamalrau Tallury, USDA). All other wild seeds were provided by GRIN’s U.S. National Plant Germplasm System (see Table 2). All rhizobia were provided by Patrick Elia, USDA Germplasm Resource Collection.

Funding

This research was funded by the National Science Foundation (DEB- 1943239 to SSP) as well as by Washington State University, Vancouver in the form of a Mini-Grant to SSP and a Natural Sciences Graduate Fellowship to NM.

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  1. School of Biological Sciences, Washington State University, 14204 NE Salmon Creek Ave, Vancouver, WA, 98686, USA

    Niall Millar, Jonah Piovia-Scott & Stephanie S. Porter

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  1. Niall Millar
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Niall Millar (NM) conducted the experiment and wrote the manuscript. Jonah Piovia-Scott assisted with the data analysis. Stephanie Porter (SSP) supervised the practical work and edited the manuscript.

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Correspondence to Stephanie S. Porter.

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11104_2023_6128_MOESM2_ESM.docx

Supplementary file2 (DOCX 104 KB) Fig. S1 Individual plant lines of domesticated field pea (Pisum sativum) and wild Pisum sativum subsp. elatius differ in their nodule/shoot mass response to N fertiliser addition. Means and standard errors of nodule/shoot mass of domesticated and wild Pisum across levels of N fertilisation. Cultivars shown in grey, wild accessions shown in black. Fig. S2 Individual plant lines of domesticated chickpea (Cicer arietinum) and wild Cicer reticulatum differ in their number of viable rhizobia per nodule in response to N fertiliser addition. Means and standard errors of colony forming units (CFU) of domesticated and wild Cicer across levels of N fertilisation. CFU per nodule is a measure of rhizobial symbiont abundance (i.e., viable bacterial cells) per nodule. Cultivars shown in grey, wild accessions shown in black.

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Millar, N., Piovia-Scott, J. & Porter, S.S. Impacts of domestication on the rhizobial mutualism of five legumes across a gradient of nitrogen-fertilisation. Plant Soil 491, 479–499 (2023). https://doi.org/10.1007/s11104-023-06128-x

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