Abstract
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.Electronic supplementary materialThe online version of this article (doi:10.1186/s12870-015-0557-7) contains supplementary material, which is available to authorized users.
Highlights
Leaf morphology varies extensively among plant species and is under strong genetic control
Identification of a major Quantitative trait locus (QTL) for leaf blade width We carried out a QTL analysis for variation in leaf lamina shape in an interspecific pseudo-backcross pedigree segregating between the narrow-leaf donor parent species P. trichocarpa and the broad-leaf recurrent parent P. deltoides (Fig. 1)
One or more significant QTL were detected using composite interval mapping (CIM) [38, 39] using a standard threshold of the 95th percentile of 1000 permutations, for all traits measured in the population of 396 individuals grown in a greenhouse at the University of Florida (Table 1)
Summary
Leaf 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 It is not known whether this diversity across plant species is related to naturally occurring variation at these genes. Few studies have directly addressed whether alternative alleles at these genes underlie variation in leaf shape within or between different plant species [11] In light of this shortcoming and the extensive diversity in leaf form, additional studies exploiting naturally occurring variation are needed to clarify the role of previously discovered genes in evolutionary variation for leaf traits and potentially discover new genetic regulators. Novel experimental approaches developed from advances in genome sequencing and transcriptome analysis have eased QTL cloning [18,19,20], making QTL-based techniques powerful tools to elucidate molecular mechanisms underlying naturally occurring phenotypic variation [21, 22]. More recently the use of genetical genomics has expanded to several plant species, to understand the genetic regulation of developmental traits [28], as well as biotic [29] and abiotic [30] stress response
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