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Leaf shape in Populus tremula is a complex, omnigenic trait.

ABSTRACT: Leaf shape is a defining feature of how we recognize and classify plant species. Although there is extensive variation in leaf shape within many species, few studies have disentangled the underlying genetic architecture. We characterized the genetic architecture of leaf shape variation in Eurasian aspen (Populus tremula L.) by performing genome-wide association study (GWAS) for physiognomy traits. To ascertain the roles of identified GWAS candidate genes within the leaf development transcriptional program, we generated RNA-Seq data that we used to perform gene co-expression network analyses from a developmental series, which is publicly available within the PlantGenIE resource. We additionally used existing gene expression measurements across the population to analyze GWAS candidate genes in the context of a population-wide co-expression network and to identify genes that were differentially expressed between groups of individuals with contrasting leaf shapes. These data were integrated with expression GWAS (eQTL) results to define a set of candidate genes associated with leaf shape variation. Our results identified no clear adaptive link to leaf shape variation and indicate that leaf shape traits are genetically complex, likely determined by numerous small-effect variations in gene expression. Genes associated with shape variation were peripheral within the population-wide co-expression network, were not highly connected within the leaf development co-expression network, and exhibited signatures of relaxed selection. As such, our results are consistent with the omnigenic model.

SUBMITTER: Mahler N

PROVIDER: S-EPMC7663049 | biostudies-literature | 2020 Nov

REPOSITORIES: biostudies-literature

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Leaf shape in <i>Populus tremula</i> is a complex, omnigenic trait.

Mähler Niklas N Schiffthaler Bastian B Robinson Kathryn M KM Terebieniec Barbara K BK Vučak Matej M Mannapperuma Chanaka C Bailey Mark E S MES Jansson Stefan S Hvidsten Torgeir R TR Street Nathaniel R NR

Ecology and evolution 20201013 21

Leaf shape is a defining feature of how we recognize and classify plant species. Although there is extensive variation in leaf shape within many species, few studies have disentangled the underlying genetic architecture. We characterized the genetic architecture of leaf shape variation in Eurasian aspen (<i>Populus tremula</i> L.) by performing genome-wide association study (GWAS) for physiognomy traits. To ascertain the roles of identified GWAS candidate genes within the leaf development transc ...[more]

PMID: 33209260

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Project description:BackgroundLeaf morphology varies extensively among plant species and is under strong genetic control. Mutagenic screens in model systems have identified genes and established molecular mechanisms regulating leaf initiation, development, and shape. However, it is not known whether this diversity across plant species is related to naturally occurring variation at these genes. Quantitative trait locus (QTL) analysis has revealed a polygenic control for leaf shape variation in different species suggesting that loci discovered by mutagenesis may only explain part of the naturally occurring variation in leaf shape. Here we undertook a genetical genomics study in a poplar intersectional pseudo-backcross pedigree to identify genetic factors controlling leaf shape. The approach combined QTL discovery in a genetic linkage map anchored to the Populus trichocarpa reference genome sequence and transcriptome analysis.ResultsA major QTL for leaf lamina width and length:width ratio was identified in multiple experiments that confirmed its stability. A transcriptome analysis of expanding leaf tissue contrasted gene expression between individuals with alternative QTL alleles, and identified an ADP-ribosylation factor (ARF) GTPase (PtARF1) as a candidate gene for regulating leaf morphology in this pedigree. ARF GTPases are critical elements in the vesicular trafficking machinery. Disruption of the vesicular trafficking function of ARF by the pharmacological agent Brefeldin A (BFA) altered leaf lateral growth in the narrow-leaf P. trichocarpa suggesting a molecular mechanism of leaf shape determination. Inhibition of the vesicular trafficking processes by BFA interferes with cycling of PIN proteins and causes their accumulation in intercellular compartments abolishing polar localization and disrupting normal auxin flux with potential effects on leaf expansion.ConclusionsIn other model systems, ARF proteins have been shown to control the localization of auxin efflux carriers, which function to establish auxin gradients and apical-basal cell polarity in developing plant organs. Our results support a model where PtARF1 transcript abundance changes the dynamics of endocytosis-mediated PIN localization in leaf cells, thus affecting lateral auxin flux and subsequently lamina leaf expansion. This suggests that evolution of differential cellular polarity plays a significant role in leaf morphological variation observed in subgenera of genus Populus.

Project description:As an important functional organ of plants, leaves alter their shapes in response to a changing environment. The variation of leaf shape has long been an important evolutionary and developmental force in plants. Despite an increasing amount of investigations into the genetic controls of leaf morphology, few have systematically studied the genetic architecture controlling shape differences among distinct altitudes. Altitude denotes a comprehensive complex of environmental factors affecting plant growth in many aspects, e.g., UV-light radiation, temperature, and humidity. To reveal how plants alter ecological adaptation to altitude through genes, we used Populus szechuanica var. tibetica growing on the Qinghai-Tibetan plateau. F ST between the low- and high- altitude population was 0.00748, Q ST for leaf width, length and area were 0.00924, 0.1108, 0.00964 respectively. With the Elliptic Fourier-based morphometric model, association study of leaf shape was allowed, the dissection of the pleiotropic expression of genes mediating altitude-derived leaf shape variation was performed. For high and low altitudes, 130 and 131 significant single-nucleotide polymorphisms (SNPs) were identified. QTLs that affected leaf axis length and leaf width were expressed in both-altitude population, while QTLs regulating "leaf tip" and "leaf base" were expressed in low-altitude population. Pkinase and PRR2 were common significant genes in both types of populations. Auxin-related and differentiation-related genes included PIN1, CDK-like, and CAK1AT at high altitude, whereas they included NAP5, PIN-LIKES, and SCL1 at low altitude. The presence of Stress-antifung gene, CIPK3 and CRPK1 in high-altitude population suggested an interaction between genes and harsh environment in mediating leaf shape, while the senescence repression-related genes (EIN2 and JMJ18) and JMT in jasmonic acid pathway in low-altitude population suggested their crucial roles in ecological adaptability. These data provide new information that strengthens the understanding of genetic control with respect to leaf shape and constitute an entirely novel perspective regarding leaf adaptation and development in plants.

Project description:BackgroundIonic aluminum (mainly Al3+) is rhizotoxic and can be present in acid soils at concentrations high enough to inhibit root growth. Many forest tree species grow naturally in acid soils and often tolerate high concentrations of Al. Previously, we have shown that aspen (Populus tremula) releases citrate and oxalate from roots in response to Al exposure. To obtain further insights into the root responses of aspen to Al, we investigated root gene expression at Al conditions that inhibit root growth.ResultsTreatment of the aspen roots with 500 ?M Al induced a strong inhibition of root growth within 6 h of exposure time. The root growth subsequently recovered, reaching growth rates comparable to that of control plants. Changes in gene expression were determined after 6 h, 2 d, and 10 d of Al exposure. Replicated transcriptome analyses using the Affymetrix poplar genome array revealed a total of 175 significantly up-regulated and 69 down-regulated genes, of which 70% could be annotated based on Arabidopsis genome resources. Between 6 h and 2 d, the number of responsive genes strongly decreased from 202 to 26, and then the number of changes remained low. The responses after 6 h were characterized by genes involved in cell wall modification, ion transport, and oxidative stress. Two genes with prolonged induction were closely related to the Arabidopsis Al tolerance genes ALS3 (for Al sensitive 3) and MATE (for multidrug and toxin efflux protein, mediating citrate efflux). Patterns of expression in different plant organs and in response to Al indicated that the two aspen genes are homologs of the Arabidopsis ALS3 and MATE.ConclusionExposure of aspen roots to Al results in a rapid inhibition of root growth and a large change in root gene expression. The subsequent root growth recovery and the concomitant reduction in the number of responsive genes presumably reflect the success of the roots in activating Al tolerance mechanisms. The aspen genes ALS3 and MATE may be important components of these mechanisms.

Dataset Information

Leaf shape in Populus tremula is a complex, omnigenic trait.

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Leaf shape in <i>Populus tremula</i> is a complex, omnigenic trait.

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