Constructing functional cuticles: analysis of relationships between cuticle lipid composition, ultrastructure and water barrier function in developing adult maize leaves

Bourgault, Richard; Matschi, Susanne; Vasquez, Miguel; Qiao, Pengfei; Sonntag, Annika; Charlebois, Caleb; Mohammadi, Marc; Scanlon, Michael J.; Smith, Laurie G.; Molina, Isabel

doi:10.1093/aob/mcz143

Cited by 66 publications

(86 citation statements)

References 76 publications

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“…The total amount of cuticular wax was estimated to be 0.91 μg cm −2 when a non-polar solvent (chloroform) was used for its extraction from intact leaves. This is in good agreement with previously published results (0.7 μg cm −2 [ 21 ]; 0.9 μg cm −2 [ 7 ]; 1.2 μg cm −2 [ 5 ]). Isolation of the cuticle led to a higher yield of extracted wax.…”

Section: Discussionsupporting

confidence: 94%

A modified method for enzymatic isolation of and subsequent wax extraction from Arabidopsis thaliana leaf cuticle

et al. 2020

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Background The plant cuticle represents one of the major adaptations of vascular plants to terrestrial life. Cuticular permeability and chemical composition differ among species. Arabidopsis thaliana is a widely used model for biochemical and molecular genetic studies in plants. However, attempts to isolate the intact cuticle from fresh leaves of Arabidopsis have failed so far. The goal of this study was to optimise an enzymatic method for cuticle isolation of species with a thin cuticle and to test it on several A. thaliana wild types and mutants. Results We developed a method for isolation of thin cuticles that allows reducing the isolation time, the separation of abaxial and adaxial cuticles, and avoids formation of wrinkles. Optical microscopy was used for studying cuticle intactness and scanning electron microscopy for visualisation of external and internal cuticle structures after isolation. Wax extracts were analysed by GC–MS. Isolation of intact cuticle was successful for all tested plants. The wax compositions (very-long-chained fatty acids, alcohols and alkanes) of intact leaves and isolated cuticles of wild type Col-0 were compared. Conclusions We conclude that the optimised enzymatic method is suitable for the isolation of A. thaliana adaxial and abaxial cuticles. The isolated cuticles are suitable for microscopic observation. Analysis of wax composition revealed some discrepancies between isolated cuticles and intact leaves with a higher yield of wax in isolated cuticles.

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Section: Discussionsupporting

confidence: 94%

A modified method for enzymatic isolation of and subsequent wax extraction from Arabidopsis thaliana leaf cuticle

et al. 2020

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“…Given that the leaf cuticle is produced by epidermal cells, we analyzed LM-RNAseq data of epidermal cells from seven 2-cm intervals excised from the expanding leaf 8 of maize inbred B73 (Qiao et al . 2019), representing sequential stages in cuticle maturation (Bourgault et al . 2019).…”

Section: Resultsmentioning

confidence: 99%

“…Of the seven promising candidate genes contributing to the genetic regulation of natural variation for g c through potential influence on cuticle development, those encoding CAP, ISTL1 protein, GDSL lipase, β-D-XYLOSIDASE 4, and the two SEC14-like proteins were found to be epidermally expressed (Figure 3), while the homolog of CER7 was not declared to be expressed in the leaf epidermis based on its transcript abundance (Table S9). In general, transcript abundance increased for the ISTL1 protein and GDSL lipase along the leaf developmental gradient from the base (youngest, 2-4 cm) towards the tip (oldest, 20-22 cm) of the leaf, with the exception of a reduced transcript abundance for GDSL lipase in the 20-22 cm interval, at which time cuticle maturation is already completed (Bourgault et al . 2019).…”

Section: Resultsmentioning

confidence: 99%

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Genome-wide association study for maize leaf cuticular conductance identifies candidate genes involved in the regulation of cuticle development

Gore

Smith

Meng

et al. 2019

Preprint

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The cuticle, a hydrophobic layer of cutin and waxes synthesized by plant epidermal cells, is the major barrier to water loss when stomata are closed at night and under water-limited conditions. Elucidating the genetic architecture of natural variation for leaf cuticular conductance (gc) is important for identifying genes relevant to improving crop productivity in drought-prone environments. To this end, we conducted a genome-wide association study of gc of adult leaves in a maize inbred association panel that was evaluated in four environments (Maricopa, AZ, and San Diego, CA in 2016 and 2017). Five genomic regions significantly associated with gc were resolved to seven plausible candidate genes (ISTL1, two SEC14 homologs, cyclase-associated protein, a CER7 homolog, GDSL lipase, and β-D-XYLOSIDASE 4). These candidates are potentially involved in cuticle biosynthesis, trafficking and deposition of cuticle lipids, cutin polymerization, and cell wall modification. Laser microdissection RNA sequencing revealed that all these candidate genes, with the exception of the CER7 homolog, were expressed in the zone of the expanding adult maize leaf where cuticle maturation occurs. With direct application to genetic improvement, moderately high average predictive abilities were observed for whole-genome prediction of gc in locations (0.46 and 0.45) and across all environments (0.52). The findings of this study provide novel insights into the genetic control of gc and have the potential to help breeders more effectively develop drought-tolerant maize for target environments. Article summary The cuticle serves as the major barrier to water loss when stomata are closed at night and under water-limited conditions and potentially relevant to drought tolerance in crops. We performed a genome-wide association study to elucidate the genetic architecture of natural variation for maize leaf cuticular conductance. We identified epidermally expressed candidate genes that are potentially involved in cuticle biosynthesis, trafficking and deposition, cutin polymerization, and cell wall modification. Finally, we observed moderately high predictive abilities for whole-genome prediction of leaf cuticular conductance. Collectively, these findings may help breeders more effectively develop drought-tolerant maize.

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“…Interestingly, long-chain alcohols (69%) are the main components of cuticular waxes in seedling leaves, followed by aldehydes (25%), alkanes (4%) and esters (2%) (Javelle et al, 2010). Differently, alkanes and alkyl esters are the main components in adult leaves (Bourgault et al, 2020). Cutin composition was characterized in adult leaves and shown to be mainly composed of dihydroxyhexadecanoic acid and typical members of the C18 family of cutin acids, including hydroxy and hydroxy-epoxy acids (Espelie and Kolattukudy, 1979).…”

Section: Discussionmentioning

confidence: 99%

The drought-responsiveZmFDL1gene regulates cuticle biosynthesis and cuticle-dependent leaf permeability

Castorina

Domergue

Chiara

et al. 2020

Preprint

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ZmFDL1 regulates cuticle-dependent leaf permeability. One-Sentence SummaryCuticle biosynthesis and cuticle-mediated drought-response during the juvenile phase of maize plant growth, are regulated by the MYB transcription factor fused leaves1 (ZmFDL1) and influenced by ABA. AbstractIn higher plants, the outer surface of the aerial parts is covered by the cuticle, a complex lipid layer that constitutes a barrier against damages caused by environmental factors and provides protection against non-stomatal water loss. We show in this study that cuticle deposition, during the juvenile phase of in maize (Zea mays) plant development, and cuticle-dependent leaf permeability are controlled by the MYB transcription factor ZmMYB94/FUSED LEAVES1 (ZmFDL1).Biochemical analysis showed that in fdl1-1 mutant seedlings at the coleoptile stage both cutin and wax biosynthesis and deposition were altered. 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, long-chain wax esters.Transcriptome analysis allowed the identification of novel candidate genes involved in lipid metabolism and the assembly of a proposed pathway for cuticle biosynthesis in maize. Lack of ZmFDL1 affects the expression of genes located in different modules of the pathway and correspondence between gene transcriptional variations and biochemical defects have been highlighted.A decrease in cuticle-dependent leaf permeability was observed in maize seedlings exposed to drought as well as ABA treatment, which implies coordinated changes in the transcript levels of ZmFDL1 and associated genes. Overall, our results suggest that the response to water stress implies the activation of wax biosynthesis and the involvement of by both ZmFDL1 and ABA regulatory pathways.

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Constructing functional cuticles: analysis of relationships between cuticle lipid composition, ultrastructure and water barrier function in developing adult maize leaves

Cited by 66 publications

References 76 publications

A modified method for enzymatic isolation of and subsequent wax extraction from Arabidopsis thaliana leaf cuticle

A modified method for enzymatic isolation of and subsequent wax extraction from Arabidopsis thaliana leaf cuticle

Genome-wide association study for maize leaf cuticular conductance identifies candidate genes involved in the regulation of cuticle development

The drought-responsiveZmFDL1gene regulates cuticle biosynthesis and cuticle-dependent leaf permeability

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