Cuticle development and the underlying transcriptome–metabolome associations during early seedling establishment

Chen, Keting; Bhunia, Rupam Kumar; Wendt, Matthew M.; Campidilli, Grace; McNinch, Colton; Hassan, Ahmed; Li, Ling; Nikolau, Basil J.; Yandeau-Nelson, Marna D.; Nakamura, ed., Yuki

doi:10.1093/jxb/erae311

Title: Cuticle development and the underlying transcriptome–metabolome associations during early seedling establishment

Journal Article · 19 July 2024 · Journal of Experimental Botany

DOI: https://doi.org/10.1093/jxb/erae311 · OSTI ID:2475439

;

; Wendt, Matthew M.; Campidilli, Grace;

; Hassan, Ahmed;

;

; Nakamura, ed., Yuki

Abstract The plant cuticle is a complex extracellular lipid barrier that has multiple protective functions. This study investigated cuticle deposition by integrating metabolomics and transcriptomics data gathered from six different maize seedling organs of four genotypes, the inbred lines B73 and Mo17, and their reciprocal hybrids. These datasets captured the developmental transition of the seedling from heterotrophic skotomorphogenic growth to autotrophic photomorphogenic growth, a transition that is highly vulnerable to environmental stresses. Statistical interrogation of these data revealed that the predominant determinant of cuticle composition is seedling organ type, whereas the seedling genotype has a smaller effect on this phenotype. Gene-to-metabolite associations assessed by integrated statistical analyses identified three gene networks associated with the deposition of different elements of the cuticle: cuticular waxes; monomers of lipidized cell wall biopolymers, including cutin and suberin; and both of these elements. These gene networks reveal three metabolic programs that appear to support cuticle deposition, including processes of chloroplast biogenesis, lipid metabolism, and molecular regulation (e.g. transcription factors, post-translational regulators, and phytohormones). This study demonstrates the wider physiological metabolic context that can determine cuticle deposition and lays the groundwork for new targets for modulating the properties of this protective barrier.

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Research Organization:: Photothermal Spectroscopy Corp., Santa Barbara, CA (United States)

Sponsoring Organization:: USDOE; USDOE Office of Science (SC)

Grant/Contract Number:: SC0018519

OSTI ID:: 2475439

Journal Information:: Journal of Experimental Botany, Journal Name: Journal of Experimental Botany Journal Issue: 20 Vol. 75; ISSN 0022-0957

Publisher:: Oxford University PressCopyright Statement

Country of Publication:: United Kingdom

Language:: English

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Genome-Wide Association Study for Maize Leaf Cuticular Conductance Identifies Candidate Genes Involved in the Regulation of Cuticle Development Lin, Meng; Matschi, Susanne; Vasquez, Miguel G3 Genes\|Genomes\|Genetics, Vol. 10, Issue 5 https://doi.org/10.1534/g3.119.400884	journal	May 2020
DLA-Based Strategies for Cloning Insertion Mutants: Cloning the gl4 Locus of Maize Using Mu Transposon Tagged Alleles Liu, Sanzhen; Dietrich, Charles R.; Schnable, Patrick S. Genetics, Vol. 183, Issue 4 https://doi.org/10.1534/genetics.109.108936	journal	December 2009
Putative Seedling Ferulate Ester () Maize Mutant: Morphology, Biomass Yield, and Stover Cell Wall Composition and Rumen Degradability Jung, H. G.; Phillips, R. L. Crop Science, Vol. 50, Issue 1 https://doi.org/10.2135/cropsci2009.04.0191	journal	January 2010
Glossy15 Controls the Epidermal Juvenile-to-Adult Phase Transition in Maize Moose, Stephen P.; Sisco, Paul H. The Plant Cell, Vol. 6, Issue 10 https://doi.org/10.2307/3869973	journal	October 1994
Similarities and Differences of Photosynthesis Establishment Related mRNAs and Novel lncRNAs in Early Seedlings (Coleoptile/Cotyledon vs. True Leaf) of Rice and Arabidopsis Shi, Yafei; Chen, Jian; Hou, Xin Frontiers in Genetics, Vol. 11 https://doi.org/10.3389/fgene.2020.565006	journal	September 2020
Identification of Hub Genes and Key Pathways Associated With Bipolar Disorder Based on Weighted Gene Co-expression Network Analysis Liu, Yang; Gu, Hui-Yun; Zhu, Jie Frontiers in Physiology, Vol. 10 https://doi.org/10.3389/fphys.2019.01081	journal	August 2019
Transcriptional regulation of thylakoid galactolipid biosynthesis coordinated with chlorophyll biosynthesis during the development of chloroplasts in Arabidopsis Kobayashi, Koichi; Fujii, Sho; Sasaki, Daichi Frontiers in Plant Science, Vol. 5 https://doi.org/10.3389/fpls.2014.00272	journal	June 2014
Chemical and structural analysis of Eucalyptus globulus and E. camaldulensis leaf cuticles: a lipidized cell wall region GuzmÃ¡n, Paula; FernÃ¡ndez, Victoria; GraÃ§a, JosÃ© Frontiers in Plant Science, Vol. 5 https://doi.org/10.3389/fpls.2014.00481	journal	September 2014
Cuticle Structure in Relation to Chemical Composition: Re-assessing the Prevailing Model Fernández, Victoria; Guzmán-Delgado, Paula; Graça, José Frontiers in Plant Science, Vol. 7 https://doi.org/10.3389/fpls.2016.00427	journal	March 2016
Transcriptional Regulation of Tetrapyrrole Biosynthesis in Arabidopsis thaliana Kobayashi, Koichi; Masuda, Tatsuru Frontiers in Plant Science, Vol. 7 https://doi.org/10.3389/fpls.2016.01811	journal	December 2016
Grass Cell Walls: A Story of Cross-Linking Hatfield, Ronald D.; Rancour, David M.; Marita, Jane M. Frontiers in Plant Science, Vol. 7 https://doi.org/10.3389/fpls.2016.02056	journal	January 2017
Genes of ACYL CARRIER PROTEIN Family Show Different Expression Profiles and Overexpression of ACYL CARRIER PROTEIN 5 Modulates Fatty Acid Composition and Enhances Salt Stress Tolerance in Arabidopsis Huang, Jiexue; Xue, Caiwen; Wang, Han Frontiers in Plant Science, Vol. 8 https://doi.org/10.3389/fpls.2017.00987	journal	June 2017
Do Galactolipid Synthases Play a Key Role in the Biogenesis of Chloroplast Membranes of Higher Plants? Rocha, Joana; Nitenberg, Milène; Girard-Egrot, Agnès Frontiers in Plant Science, Vol. 9 https://doi.org/10.3389/fpls.2018.00126	journal	February 2018
Multifunctional Roles of Plant Cuticle During Plant-Pathogen Interactions Ziv, Carmit; Zhao, Zhenzhen; Gao, Yu G. Frontiers in Plant Science, Vol. 9 https://doi.org/10.3389/fpls.2018.01088	journal	July 2018
MADS-Box Genes Are Key Components of Genetic Regulatory Networks Involved in Abiotic Stress and Plastic Developmental Responses in Plants Castelán-Muñoz, Natalia; Herrera, Joel; Cajero-Sánchez, Wendy Frontiers in Plant Science, Vol. 10 https://doi.org/10.3389/fpls.2019.00853	journal	July 2019
Unraveling Cuticle Formation, Structure, and Properties by Using Tomato Genetic Diversity Petit, Johann; Bres, Cécile; Reynoud, Nicolas Frontiers in Plant Science, Vol. 12 https://doi.org/10.3389/fpls.2021.778131	journal	November 2021
The Complex Architecture of Plant Cuticles and Its Relation to Multiple Biological Functions Reynoud, Nicolas; Petit, Johann; Bres, Cécile Frontiers in Plant Science, Vol. 12 https://doi.org/10.3389/fpls.2021.782773	journal	December 2021
Modification of plant cell walls with hydroxycinnamic acids by BAHD acyltransferases Chandrakanth, Niharika Nonavinakere; Zhang, Chengcheng; Freeman, Jackie Frontiers in Plant Science, Vol. 13 https://doi.org/10.3389/fpls.2022.1088879	journal	January 2023
Identification of Fatty Acid Desaturases in Maize and Their Differential Responses to Low and High Temperature Zhao, Xunchao; Wei, Jinpeng; He, Lin Genes, Vol. 10, Issue 6 https://doi.org/10.3390/genes10060445	journal	June 2019
Suberin Biosynthesis, Assembly, and Regulation Woolfson, Kathlyn N.; Esfandiari, Mina; Bernards, Mark A. Plants, Vol. 11, Issue 4 https://doi.org/10.3390/plants11040555	journal	February 2022

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