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, 110 (37), 15133-8

Integration of Responses Within and Across Arabidopsis Natural Accessions Uncovers Loci Controlling Root Systems Architecture

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Integration of Responses Within and Across Arabidopsis Natural Accessions Uncovers Loci Controlling Root Systems Architecture

Ulises Rosas et al. Proc Natl Acad Sci U S A.

Abstract

Phenotypic plasticity is presumed to be involved in adaptive change toward species diversification. We thus examined how candidate genes underlying natural variation across populations might also mediate plasticity within an individual. Our implementation of an integrative "plasticity space" approach revealed that the root plasticity of a single Arabidopsis accession exposed to distinct environments broadly recapitulates the natural variation "space." Genome-wide association mapping identified the known gene PHOSPHATE 1 (PHO1) and other genes such as Root System Architecture 1 (RSA1) associated with differences in root allometry, a highly plastic trait capturing the distribution of lateral roots along the primary axis. The response of mutants in the Columbia-0 background suggests their involvement in signaling key modulators of root development including auxin, abscisic acid, and nitrate. Moreover, genotype-by-environment interactions for the PHO1 and RSA1 genes in Columbia-0 phenocopy the root allometry of other natural variants. This finding supports a role for plasticity responses in phenotypic evolution in natural environments.

Keywords: GWAS; GxE interaction; QTL; RootScape; morphometrics.

Conflict of interest statement

The authors declare no conflict of interest.

Figures

Fig. 1.
Fig. 1.
Root architecture plasticity within an accession (Col-0) broadly recapitulates natural variation quantified across 69 accessions. (A) Root phenotypes of Col-0 plants were grown under five conditions: IAA, CK, ABA, KNO3, and NH4Cl plus a control (KCl); roots of three treatment conditions are shown. (B) Root variation between 69 accessions grown under one condition (KNO3). (C) Landmark template to capture the root system architecture (11). Primary landmarks (black circles) are defined according to corresponding features in all roots; secondary landmarks (white circles) are evenly spaced between primary landmarks (11). (D) Two PCs capture more than 75% of the variation both within Col-0 (PCCOL) and between accessions (PCVAR). PC1COL and PC2COL have high correlation to PC1VAR and PC2VAR, respectively. PC1COL is mainly a size effect, whereas PC2COL captures mainly root allometry, the length and distribution of lateral roots long the primary root. SD, standard deviation.
Fig. 2.
Fig. 2.
Root plasticity variation within an accession (Col-0) spans a range of plasticity exhibited by Arabidopsis natural variants and maps to regions in chromosome III and IV. (A and B) Bars indicate SE. Red bars, Col-0 in the five treatments IAA, CK, ABA, KNO3, and NH4Cl and a KCl control (n = 20); gray bars, phenotypes of 69 Arabidopsis accessions grown under a single (KNO3) condition (n = 3–4); blue bars, reference Col-0 accession. Morphometrics modeled root systems architecture phenotypes; those corresponding to extreme root PC1COL and PC2COL phenotypes are shown. (C) Manhattan plot illustrating the GWAS mapping of the PC2COL phenotype.
Fig. 3.
Fig. 3.
Candidate genes have PC2COL mutant phenotypes; PHO1/At3g23430 and RSA1/At4g28410 show G × E interaction for KNO3, ABA, and IAA conditions. (A) PC2COL values of mutant alleles for six candidate genes (n = 22–31) grown in KNO3 media plates, compared with wild-type Col-0 (n = 36). (B) Quantitative PCR on the rsa1-1 gain-of-function mutant allele (n = 3). (CE) Reaction norms testing G × E interactions for IAA, ABA, CK, KNO3, and NH4Cl in pho1-2, rsa1-1 gain-, and rsa1-2 loss- of function mutants, respectively (n ≥ 11). Only significant interactions (KNO3, ABA, and IAA) are shown: *P < 0.05, **P < 0.005, ***P < 0.0005. Error bars: SE.
Fig. 4.
Fig. 4.
The PHO1-RSA1-dependent G × E interaction expands the root plasticity space of Col-0 to phenocopy a range of natural accessions. (A) Axis representing natural variation on PC2COL phenotype with examples of accession’s positions and root allometry phenotypes. (B) Treatments with KNO3 ABA, or IAA in rsa1-1 gain-of-function (OX) and rsa1-2 loss-of-function (KO) mutants have contrasting effects to Col-0. (C) Col-0 and rsa1 mutant alleles treated with KNO3, ABA, or IAA phenocopy the root architecture of natural variants.

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