The genetic basis of the economic spectrum of roots in a perennial grass

Importance

Plants have developed various root forms and functions in the earth’s environment, but only certain types of trait combinations have been shown to be evolutionarily viable. Using a genetic mapping population of native switchgrass, our study demonstrates multiple genetic links between root morphology, growth, and turnover. Switching from alleles derived from ecotypes of southern origin to alleles of ecotypes of northern origin increases root turnover but reduces tissue investment in root length construction. The genetic compromise between construction and renewal probably facilitates local adaptation of root strategy along hot to cold climatic gradients of the species’ range. In practice, our study provides genetic evidence that increasing the yield of switchgrass for bioenergy does not directly conflict with improving its sequestration of root-derived carbon.

Abstract

The economics of plant root building show predictable relationships with root growth, death, and nutrient uptake strategies. Plant taxa with inexpensively constructed roots tend to explore nutrient hotspots more precisely than those with expensive constructed roots, but at the cost of more frequent tissue turnover. This compromise underlies an acquisitive to conservative continuum in investing in resources, described as the “root economic spectrum (RES)”. Yet the adaptive role and genetic basis of RES remain largely uncertain. Different ecotypes of switchgrass (Panicum virgatum) exhibit root characteristics exemplifying SER, with expensive built roots in the southern lowlands and inexpensively built roots in northern highland ecotypes. We used an outbred genetic mapping population derived from lowland and highland switchgrass ecotypes to examine the genetic architecture of RES. We found that the absorbing roots (distal first and second order) were often “deciduous” in winter. The percentage of winter-absorbing roots was decreased by northern highland alleles compared to southern lowland alleles, suggesting a conservative strategy adapted locally in a warmer and acquisition strategy in colder regions. The relative turnover of absorbent roots was genetically negatively correlated with their investment in biomass per unit of root length, suggesting that the key trade-off in the regulation of RES is genetically facilitated. We also detected strong genetic correlations between root morphology, root productivity and shoot size. Overall, our results reveal the genetic architecture of several traits that likely impact the evolution of RES and the air-subsoil organization of plants. In practice, we provide genetic evidence that increasing the yield of switchgrass for bioenergy does not directly conflict with improving its sequestration of carbon derived from the roots.

Footnotes

    • Accepted October 9, 2021.
  • Author contributions: research designed by WC and TEJ; WC researched and analyzed the data; and WC, YW, FBF and TEJ wrote the article.

  • The authors declare no competing interests.

  • This article is a direct PNAS submission.

  • This article contains additional information online at https://www.pnas.org/lookup/suppl/doi:10.1073/pnas.2107541118/-/DCSupplemental.

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