The epidermis coordinates auxin-induced stem growth in response to shade

Abstract

Growth of a complex multicellular organism requires coordinated changes in diverse cell types. These cellular changes generate organs of the correct size, shape, and functionality. In plants, the growth hormone auxin induces stem elongation in response to shade; however, which cell types of the stem perceive the auxin signal and contribute to organ growth is poorly understood. Here, we blocked the transcriptional response to auxin within specific tissues to show that auxin signaling is required in many cell types for correct hypocotyl growth in shade, with a key role for the epidermis. Combining genetic manipulations in Arabidopsis thaliana with transcriptional profiling of the hypocotyl epidermis from Brassica rapa, we show that auxin acts in the epidermis in part by inducing activity of the locally acting, growth-promoting brassinosteroid pathway. Our findings clarify cell-specific auxin function in the hypocotyl and highlight the complexity of cell type interactions within a growing organ.

Neighbor Detection Induces Organ-Specific Transcriptomes, Revealing Patterns Underlying Hypocotyl-Specific Growth

“…These data indicate that many early shade-regulated genes are bound by PIFs and ARFs, showing that, as observed in other growth-stimulating conditions (Oh et al, 2014), many genes are bound by both classes of transcription factors in response to shade (Figure 3). Furthermore, consistent with the role of BL in multiple growth responses (Oh et al, 2014;Das et al, 2016;Procko et al, 2016), we also detected BZR1 binding to many rapidly shade-regulated genes ( Figure 3).…”

“…These expression patterns suggest a rise in BL levels in hypocotyls, which is consistent with the positive correlation between expression patterns triggered by BL and shade, specifically in hypocotyls ( Figure 2E). The functional importance of DWF4 and BAS1 in this process was shown genetically, suggesting that local BL homeostasis contributes to selective hypocotyl elongation (Figure 2) (Das et al, 2016;Procko et al, 2016). Similarly, the hypocotyl-specific induction of AtGA3ox1 that we report here ( Figure 2D; Supplemental Figure 2D and Supplemental Data Set 2), together with the requirement of AtGA3ox1 for normal shadeinduced hypocotyl elongation (Yu et al, 2015), suggest a role for GA in selective growth enhancement of this organ.…”

“…Low R/FR releases phyB-mediated inhibition of several PIFs, leading to shade-induced elongation of hypocotyls and petioles (Lorrain et al, 2008;Keller et al, 2011;Leivar et al, 2012;Li et al, 2012;de Wit et al, 2015;Mizuno et al, 2015;Nozue et al, 2015). Shade-induced auxin biosynthesis in the cotyledons and young leaves followed by transport of the phytohormone into the hypocotyl is considered essential to trigger hypocotyl elongation (Steindler et al, 1999;Tao et al, 2008;Keuskamp et al, 2010;de Wit et al, 2014;Procko et al, 2014Procko et al, , 2016. In response to shade, PIF transcription factors directly regulate the expression of auxin biosynthesis and auxin response genes, thereby providing a link between environmental perception and the growth response (Hornitschek et al, 2012;Li et al, 2012;Hersch et al, 2014;Nozue et al, 2015).…”

“…In particular, brassinosteroids, gibberellic acid (GA), and jasmonic acid have been shown to function in growth regulation in shaded environments (DjakovicPetrovic et al, 2007;Kozuka et al, 2010;Robson et al, 2010;Keller et al, 2011;Keuskamp et al, 2011;Cifuentes-Esquivel et al, 2013;Bou-Torrent et al, 2014;Moreno and Ballaré, 2014;Nozue et al, 2015;Das et al, 2016;Procko et al, 2016). Abscisic acid (ABA), cytokinins, and ethylene have also been linked to a subset of shaderegulated responses (Carabelli et al, 2007;Pierik et al, 2009;Reddy et al, 2013;Zheng et al, 2013;Pierik and Testerink, 2014).…”

Local auxin production underlies a spatially restricted neighbor-detection response inArabidopsis

“…Moreover, auxin signaling in the epidermis is important to control low R/FR-induced hypocotyl elongation (43), suggesting that auxin signaling in the epidermis is important to mediate shade-induced leaf hyponasty. To test this notion we used epidermal-specific expression of axr3-1 (CER6:axr3-1), coding for a stable version of the IAA17 auxinsignaling inhibitor (43). In this mutant leaf movements were altered in control conditions, and low R/FR-induced leaf hyponasty was largely suppressed (Fig.…”