Light-induced indeterminacy alters shade avoiding tomato leaf morphology

Abstract

Plants sense the foliar shade of competitors and alter their developmental programs through the shade-avoidance response. Internode and petiole elongation, and changes in overall leaf area and leaf mass per area, are the stereotypical architectural responses to foliar shade in the shoot. However, changes in leaf shape and complexity in response to shade remain incompletely, and qualitatively, described. Using a meta-analysis of more than 18,000 previously published leaflet outlines, we demonstrate that shade avoidance alters leaf shape in domesticated tomato (Solanum lycopersicum) and wild relatives. The effects of shade avoidance on leaf shape are subtle with respect to individual traits but are combinatorially strong. We then seek to describe the developmental origins of shade-induced changes in leaf shape by swapping plants between light treatments. Leaf size is light responsive late into development, but patterning events, such as stomatal index, are irrevocably specified earlier. Observing that shade induces increases in shoot apical meristem size, we then describe gene expression changes in early leaf primordia and the meristem using laser microdissection. We find that in leaf primordia, shade avoidance is not mediated through canonical pathways described in mature organs but rather through the expression of KNOTTED1-LIKE HOMEOBOX and other indeterminacy genes, altering known developmental pathways responsible for patterning leaf shape. We also demonstrate that shade-induced changes in leaf primordium gene expression largely do not overlap with those found in successively initiated leaf primordia, providing evidence against classic hypotheses that shaded leaf morphology results from the prolonged production of juvenile leaf types.

Climate and Developmental Plasticity: Interannual Variability in Grapevine Leaf Morphology

“…Thus, the timing of the types of leaves a plant displays is unaffected (Jones, 1995). This interpretation is also supported by recent work analyzing the transcriptomic responses in leaf primordia to simulated foliar shade and heteroblasty, showing that these phenomena in tomato leaf primordia are largely distinct at the molecular level (Chitwood et al, 2015a). Environmentally induced changes in leaf shape through timing-dependent (heterochronic) or timing-independent mechanisms are important, since field-based observations demonstrate that leaves plastically respond to their climate (Royer et al, 2009).…”

“…Environmentally induced changes in leaf shape through timing-dependent (heterochronic) or timing-independent mechanisms are important, since field-based observations demonstrate that leaves plastically respond to their climate (Royer et al, 2009). This plasticity often results in changes to marginal serrations and lobes that are morphological features explicitly modulated by heteroblastic pathways at the molecular level in the Brassicaceae (Rubio-Somoza et al, 2014), tomato (Solanum lycopersicum; Chitwood et al, 2015a), and Proteaceae (Ostria-Gallardo et al, 2015). Extant species distributions and the paleobotanical record attest to changes in these features during the evolution of flowering plants, especially long-lived woody perennials Sinnott, 1915, 1916;Webb, 1968;Wolfe, 1978Wolfe, , 1979Wolfe, , 1993Wolfe, , 1995Givnish, 1979Givnish, , 1984Hall and Swaine, 1981;Richards, 1996;Wilf, 1997;Wilf et al, 1998;Jacobs, 1999Jacobs, , 2002Feild et al, 2005;Traiser et al, 2005;Royer and Wilf, 2006;Peppe et al, 2011).…”

eQTL Regulating Transcript Levels Associated with Diverse Biological Processes in Tomato

“…6D). We previously showed that genes with high P1 transcript levels are enriched for photosynthetic-related GO terms compared to SAM/P0 genes enriched for transcription, cell division, and epigenetics-related GO terms (Chitwood et al, 2015), suggesting a genetic basis at both a functional and tissue-specific level for genes related to photosynthesis expressed preferentially in the P1 compared to the SAM/P0.…”

“…We also analyzed hand dissected samples of the SAM + P0-P4 vs. the P5 collected over time (Fig. 6, B and C), representing genes regulated by vegetative phase change (heteroblasty; Chitwood et al, 2015).…”

“…Differentially expressed genes with enriched transcript levels in lasermicrodissected SAM/P0 versus P1 samples or hand-dissected samples of the SAM + P0-P4 or P5 sampled over developmental time were obtained from Chitwood et al (2015). Genes for which a differential expression call could be made (i.e.…”