Repeated Evolutionary Changes of Leaf Morphology Caused by Mutations to a Homeobox Gene

Sicard, Adrien; Thamm, Anna; Marona, Cindy; Lee, Young Wha; Wahl, Vanessa; Stinchcombe, John R.; Wright, Stephen I.; Kappel, Christian; Lenhard, Michael

doi:10.1016/j.cub.2014.06.061

Cited by 110 publications

(121 citation statements)

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“…Of the four genes, Gorai.002G244200 (hereafter GhLMI1-D1a) and Gorai.002G244000 (hereafter GhLMI1-D1b) are paralogues coding for HD-Zip transcription factors with 71.2% protein similarity. Their homologs were implicated in flowering time and leaf complexity in Arabidopsis (8,9,35). Of the remaining two putative genes, Gorai002G244100 (hereafter GhRLK1) is a serine/ threonine protein kinase, whereas Gorai.002G243900 (hereafter GhHRA1) is a trihelix transcription factor.…”

Section: Resultsmentioning

confidence: 99%

“…As the primary sources of photoassimilate in the world's major crops, the role of leaves-their shapes, the constraints morphology places on other physiologically relevant features, and the contributions of leaf shape to canopy and plant architecture-whether directly or indirectly selected upon during domestication, is an indisputably important consideration when discussing agricultural productivity. Although much is known about the developmental genetic basis of leaf morphology, only a handful of genes modifying leaf shapes in crops or responsible for natural variation among species have been identified (5)(6)(7)(8)(9)(10).…”

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confidence: 99%

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Modifications to a LATE MERISTEM IDENTITY1 gene are responsible for the major leaf shapes of Upland cotton ( Gossypium hirsutum L.)

Andres

Coneva

Frank

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

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Leaf shape varies spectacularly among plants. Leaves are the primary source of photoassimilate in crop plants, and understanding the genetic basis of variation in leaf morphology is critical to improving agricultural productivity. Leaf shape played a unique role in cotton improvement, as breeders have selected for entire and lobed leaf morphs resulting from a single locus, okra (L-D 1 ), which is responsible for the major leaf shapes in cotton. The L-D 1 locus is not only of agricultural importance in cotton, but through pioneering chimeric and morphometric studies, it has contributed to fundamental knowledge about leaf development. Here we show that an HD-Zip transcription factor homologous to the LATE MERISTEM IDENTITY1 (LMI1) gene of Arabidopsis is the causal gene underlying the L-D 1 locus. The classical okra leaf shape allele has a 133-bp tandem duplication in the promoter, correlated with elevated expression, whereas an 8-bp deletion in the third exon of the presumed wild-type normal allele causes a frame-shifted and truncated coding sequence. Our results indicate that subokra is the ancestral leaf shape of tetraploid cotton that gave rise to the okra allele and that normal is a derived mutant allele that came to predominate and define the leaf shape of cultivated cotton. Virusinduced gene silencing (VIGS) of the LMI1-like gene in an okra variety was sufficient to induce normal leaf formation. The developmental changes in leaves conferred by this gene are associated with a photosynthetic transcriptomic signature, substantiating its use by breeders to produce a superior cotton ideotype. cotton | leaf shape | okra | gene cloning

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Section: Resultsmentioning

confidence: 99%

mentioning

confidence: 99%

Modifications to a LATE MERISTEM IDENTITY1 gene are responsible for the major leaf shapes of Upland cotton ( Gossypium hirsutum L.)

Andres

Coneva

Frank

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

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“…The REDUCED COMPLEXITY (RCO) gene played a key role in leaf shape diversification in the crucifer family (Sicard et al 2014;Vlad et al 2014), to which the reference plant Arabidopsis thaliana belongs. RCO arose through gene duplication and encodes a class I homeobox leucine zipper protein.…”

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confidence: 99%

Coupled enhancer and coding sequence evolution of a homeobox gene shaped leaf diversity

et al. 2016

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Here we investigate mechanisms underlying the diversification of biological forms using crucifer leaf shape as an example. We show that evolution of an enhancer element in the homeobox gene REDUCED COMPLEXITY (RCO) altered leaf shape by changing gene expression from the distal leaf blade to its base. A single amino acid substitution evolved together with this regulatory change, which reduced RCO protein stability, preventing pleiotropic effects caused by its altered gene expression. We detected hallmarks of positive selection in these evolved regulatory and coding sequence variants and showed that modulating RCO activity can improve plant physiological performance. Therefore, interplay between enhancer and coding sequence evolution created a potentially adaptive path for morphological evolution.Supplemental material is available for this article.Received September 29, 2016; revised version accepted October 25, 2016. Understanding the genetic basis for evolutionary change is a fundamental problem in biology. Morphological diversity is often underpinned by cis-regulatory divergence of developmental genes and consequent spatiotemporal modification of their expression (Gompel et al. 2005;Hay and Tsiantis 2006;Prud'homme et al. 2006;Carroll 2008;Chan et al. 2010;Frankel et al. 2011;Studer et al. 2011;Arnoult et al. 2013;Rast-Somssich et al. 2015;Indjeian et al. 2016). However, the origin of specific cisregulatory elements underlying morphological diversity is still poorly understood (Rebeiz et al. 2015). For example, it is unclear whether such cis elements tend to arise de novo from rapidly evolving sequences or through the cooption of existing conserved regulatory sequences (Rebeiz et al. 2011;Boyd et al. 2015;Villar et al. 2015). Furthermore, it has not been investigated whether and how coding sequences evolve in concert with regulatory changes to optimize gene function in a new expression domain. Finally, links between regulatory changes underlying morphological change and organismal physiology and fitness remain scarce.Plant leaves present a useful genetic model to tackle these questions because they show substantial morphological variation (Shleizer-Burko et al. 2011;Bar and Ori 2014) and have considerable eco-physiological importance as the major site of photosynthetic carbon fixation in terrestrial ecosystems (Givnish 1978). The REDUCED COMPLEXITY (RCO) gene played a key role in leaf shape diversification in the crucifer family (Sicard et al. 2014;Vlad et al. 2014), to which the reference plant Arabidopsis thaliana belongs. RCO arose through gene duplication and encodes a class I homeobox leucine zipper protein.Its function was discovered in Cardamine hirsuta, where it acts to divide the leaf into distinct leaflets by locally repressing growth at the leaf margin, creating a complex shape. This species-specific activity of RCO arose by neofunctionalization following gene duplication of its ancestral paralog, LMI1, which is conserved in seed plants. Specifically, RCO acquired a novel expression domain within...

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“…Another recent work compared the level of leaf dissection in various species of the genus Capsella and found that diversification in the RCO paralogs can account for naturally occurring leaf-shape variation in this Brassicaceae family. RCO expression can be temperature responsive in some cases, which is possibly involved in the plasticity of leaf shape under different temperatures (Sicard et al, 2014). In both Capsella and C. hirsuta, differential expression rather than protein function is thought to account for the evolution of the function in leaf complexity.…”

Section: Marginal Patterning In Simple and Compound Leavesmentioning

confidence: 99%

Leaf development and morphogenesis

2014

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The development of plant leaves follows a common basic program that is flexible and is adjusted according to species, developmental stage and environmental circumstances. Leaves initiate from the flanks of the shoot apical meristem and develop into flat structures of variable sizes and forms. This process is regulated by plant hormones, transcriptional regulators and mechanical properties of the tissue. Here, we review recent advances in the understanding of how these factors modulate leaf development to yield a substantial diversity of leaf forms. We discuss these issues in the context of leaf initiation, the balance between morphogenesis and differentiation, and patterning of the leaf margin.

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Repeated Evolutionary Changes of Leaf Morphology Caused by Mutations to a Homeobox Gene

Cited by 110 publications

References 36 publications

Modifications to a LATE MERISTEM IDENTITY1 gene are responsible for the major leaf shapes of Upland cotton ( Gossypium hirsutum L.)

Modifications to a LATE MERISTEM IDENTITY1 gene are responsible for the major leaf shapes of Upland cotton ( Gossypium hirsutum L.)

Coupled enhancer and coding sequence evolution of a homeobox gene shaped leaf diversity

Leaf development and morphogenesis

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