Drought-Responsive ZmFDL1/MYB94 Regulates Cuticle Biosynthesis and Cuticle-Dependent Leaf Permeability.

Giulia Castorina,Gabriella Consonni,Frédéric Domergue,Martina Persico,Massimo Zilio,Matteo Chiara,Valentina Ricciardi,David Stephen Horner

doi:10.1104/pp.20.00322

Giulia Castorina, Gabriella Consonni + Show 6 more

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https://doi.org/10.1104/pp.20.00322

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Abstract

In all land plants, the outer surface of aerial parts is covered by the cuticle, a complex lipid layer that constitutes a barrier against damage caused by environmental factors and provides protection against nonstomatal water loss. We show in this study that both cuticle deposition and cuticle-dependent leaf permeability during the juvenile phase of plant development are controlled by the maize (Zea mays) transcription factor ZmFUSED LEAVES 1 (FDL1)/MYB94. Biochemical analysis showed altered cutin and wax biosynthesis and deposition in fdl1-1 mutant seedlings at the coleoptile stage. Among cutin compounds, ω-hydroxy fatty acids and polyhydroxy-fatty acids were specifically affected, while the reduction of epicuticular waxes was mainly observed in primary long chain alcohols and, to a minor extent, in long-chain wax esters. Transcriptome analysis allowed the identification of candidate genes involved in lipid metabolism and the assembly of a proposed pathway for cuticle biosynthesis in maize. Lack of ZmFDL1/MYB94 affects the expression of genes located in different modules of the pathway, and we highlighted the correspondence between gene transcriptional variations and biochemical defects. We observed a decrease in cuticle-dependent leaf permeability in maize seedlings exposed to drought as well as abscisic acid treatment, which implies coordinated changes in the transcript levels of ZmFDL1/MYB94 and associated genes. Overall, our results suggest that the response to water stress implies the activation of wax biosynthesis and the involvement of both ZmFDL1/MYB94 and abscisic acid regulatory pathways.

Highlights

In higher plants, the outer surface of aerial parts, including vegetative organs, flowers, fruits, seeds and pollen grains, is constituted by a continuous hydrophobic layer termed cuticle, which consists of two major components, the polymer cutin and cuticular waxes
The first phase of wax biosynthesis consists in the elongation of C16 and C18 fatty acids produced in the plastids to very-long-chain fatty acids (VLCFAs), with a chain length between C22 and C38, by elongase (FAE) complexes in the endoplasmic reticulum (Haslam and Kunst, 2013)
Loss of ZmMYB94/FUSED LEAVES1 (ZmFDL1) activity had no substantial effect on the very-long-chain fatty acids (VLCFA) and fatty alcohols (Fig 1C) as only a few monomers were significantly different from wild type at the early stage of seedling development (Supplemental Fig. S2A, B)

Summary

Introduction

The outer surface of aerial parts, including vegetative organs, flowers, fruits, seeds and pollen grains, is constituted by a continuous hydrophobic layer termed cuticle, which consists of two major components, the polymer cutin and cuticular waxes. Cutin monomers are synthetized in the endoplasmic reticulum (ER), through different reactions, including the esterification of fatty acids to coenzyme A (CoA), ω-hydroxylation and further oxidation, glycerol-3-. Cuticular waxes are constituted by a complex mixture of very-long-chain fatty acids (VLCFAs), with more than 20 carbon atoms, and their derivatives, which include alcohols, aldehydes, alkanes, ketones and wax esters. They include variable amounts of cyclic compounds, such as triterpenoids and phenylpropanoids (Bernard and Joubès, 2013; Lee and Suh, 2015a).

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