Local auxin metabolism regulates environment-induced hypocotyl elongation

Abstract

A hallmark of plants is their adaptability of size and form in response to widely fluctuating environments. The metabolism and redistribution of the phytohormone auxin play pivotal roles in establishing active auxin gradients and resulting cellular differentiation. In Arabidopsis thaliana, cotyledons and leaves synthesize indole-3-acetic acid (IAA) from tryptophan through indole-3-pyruvic acid (3-IPA) in response to vegetational shade. This newly synthesized auxin moves to the hypocotyl where it induces elongation of hypocotyl cells. Here we show that loss of function of VAS2 (IAA-amido synthetase Gretchen Hagen 3 (GH3).17) leads to increases in free IAA at the expense of IAA-Glu (IAA-glutamate) in the hypocotyl epidermis. This active IAA elicits shade- and high temperature-induced hypocotyl elongation largely independently of 3-IPA-mediated IAA biosynthesis in cotyledons. Our results reveal an unexpected capacity of local auxin metabolism to modulate the homeostasis and spatial distribution of free auxin in specialized organs such as hypocotyls in response to shade and high temperature.

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

“…The expression of members of the SAUR19 subfamily of early auxin-responsive genes (Chapman et al, 2012;Spartz et al, 2012) is very rapidly shade induced in hypocotyls, and SAUR22 induction still occurs in the pin3 pin4 pin7 and yuc2 yuc5 yuc8 yuc9 mutants, suggesting the involvement of a local response ( Figure 4). The rapid induction of SAUR22 could be due to locally regulated auxin homeostasis (Zheng et al, 2016). Consistent with such a possibility, we found that DII-VENUS levels declined in the hypocotyls of shade-treated pin3 pin4 pin7 seedlings (Supplemental Figure 4H).…”

“…Although shade-induced hypocotyl elongation requires an interaction between cotyledons and hypocotyls (see above), some shade responses occur in an organ-autonomous manner (Morgan et al, 1980;Procko et al, 2014;Nito et al, 2015;Zheng et al, 2016). The expression of members of the SAUR19 subfamily of early auxin-responsive genes (Chapman et al, 2012;Spartz et al, 2012) is very rapidly shade induced in hypocotyls, and SAUR22 induction still occurs in the pin3 pin4 pin7 and yuc2 yuc5 yuc8 yuc9 mutants, suggesting the involvement of a local response ( Figure 4).…”

Arabidopsis thaliana GH3.5 acyl acid amido synthetase mediates metabolic crosstalk in auxin and salicylic acid homeostasis

“…As described for the AtGH3.5 gain-of-function mutants and overexpression of other IAA-conjugating GH3 proteins in Arabidopsis and rice (16,17,20,(29)(30)(31), AtGH3.5 overexpression decreased IAA and increased IAA-Asp levels (Fig. 4 A and B).…”

“…Investigations of the biological action of GH3 proteins from a variety of plants have focused largely on JA and IAA; however, biochemical and structural studies suggest that the functional diversity of the GH3 protein family may be wider than previously understood. Of the 19 GH3 proteins in A. thaliana, one is required for JA-Ile biosynthesis, six are associated with conjugation and inactivation of IAA, and the rest either lack a physiological substrate or remain to be characterized (3,7,(15)(16)(17)(18)(19)(20). Of these proteins, AtGH3.5 was proposed to have a dual role in IAA and SA homeostasis (16,17).…”

“…In Arabidopsis, six GH3 proteins, AtGH3.1 (7), AtGH3.2/YDK1 (15), AtGH3.5/WES1 (16,17), AtGH3.6/DFL1 (18), AtGH3.9 (19), and AtGH3.17/VAS2 (20), are linked to IAA activity in plant growth and development. Of these proteins, AtGH3.5 is also implicated in salicylic acid (SA)-linked pathogen responses.…”