Multiple Loci Control Variation in Plasticity to Foliar Shade Throughout Development in Arabidopsis thaliana

Abstract

The shade avoidance response is a set of developmental changes exhibited by plants to avoid shading by competitors, and is an important model of adaptive plant plasticity. While the mechanisms of sensing shading by other plants are well-known and appear conserved across plants, less is known about the developmental mechanisms that result in the diverse array of morphological and phenological responses to shading. This is particularly true for traits that appear later in plant development. Here we use a nested association mapping (NAM) population of Arabidopsis thaliana to decipher the genetic architecture of the shade avoidance response in late-vegetative and reproductive plants. We focused on four traits: bolting time, rosette size, inflorescence growth rate, and inflorescence size, found plasticity in each trait in response to shade, and detected 17 total QTL; at least one of which is a novel locus not previously identified for shade responses in Arabidopsis. Using path analysis, we dissected each colocalizing QTL into direct effects on each trait and indirect effects transmitted through direct effects on earlier developmental traits. Doing this separately for each of the seven NAM populations in each environment, we discovered considerable heterogeneity among the QTL effects across populations, suggesting allelic series at multiple QTL or interactions between QTL and the genetic background or the environment. Our results provide insight into the development and variation in shade avoidance responses in Arabidopsis, and emphasize the value of directly modeling the relationships among traits when studying the genetics of complex developmental syndromes.

Functional analysis of PHYB polymorphisms in Arabidopsis thaliana collected in Patagonia

“…Together these results suggest that the SAR includes complex traits associated with the genetic background in combination with the environmental circumstances experienced by plants. Similar conclusions arrived after studying the genetic architecture of SARs in latevegetative and reproductive traits using a NAM population of Arabidopsis plants (Ta et al, 2020).…”

“…These results reflect the relevance of the genetic background and the environmental context for the expression of the QTL. More recently, a study with a NAM population of Arabidopsis plants highlights the importance of an integrated view of the genotype–phenotype relationship accounting for genetics and environment together with phenotype relationships among shade avoidance traits throughout time ( Ta et al, 2020 ).…”

“…Latitudinal origin of natural populations of Cardamine is also responsible for differences in light sensitivities being higher latitude species more sensitive to red light than lower latitude sister ( Ikeda et al, 2021 ). The genetic architecture of the SARs has been deciphered through quantitative genetics using mapping populations such as recombinant inbred lines (RILs), nested association mapping (NAM) population ( Ta et al, 2020 ), or genome-wide association study ( Filiault and Maloof, 2012 ). By Quantitative Trait Loci (QTL) mapped in different RIL populations, several studies have proposed candidate genes for SARs ( Jiménez-Gómez et al, 2010 ; Coluccio et al, 2011 ; Kasulin et al, 2013 ; Jiang et al, 2019 ; Ta et al, 2020 ).…”

“…The genetic architecture of the SARs has been deciphered through quantitative genetics using mapping populations such as recombinant inbred lines (RILs), nested association mapping (NAM) population ( Ta et al, 2020 ), or genome-wide association study ( Filiault and Maloof, 2012 ). By Quantitative Trait Loci (QTL) mapped in different RIL populations, several studies have proposed candidate genes for SARs ( Jiménez-Gómez et al, 2010 ; Coluccio et al, 2011 ; Kasulin et al, 2013 ; Jiang et al, 2019 ; Ta et al, 2020 ). For example, PHYB has been associated as a gene candidate to detect low plant density in the Ler × No-0 and Ler × Cvi RIL populations ( Botto and Coluccio, 2007 ), and ELF3 was documented as the SAR causal gene for hypocotyl growth and flowering in the Bay × Sha RIL population ( Jiménez-Gómez et al, 2010 ; Coluccio et al, 2011 ).…”