The hydrophobic cuticle of plant shoots serves as an important interaction interface with the environment. It consists of the lipid polymer cutin, embedded with and covered by waxes, and provides protection against stresses including desiccation, UV radiation, and pathogen attack. Bulliform cells form in longitudinal strips on the adaxial leaf surface, and have been implicated in the leaf rolling response observed in drought‐stressed grass leaves. In this study, we show that bulliform cells of the adult maize leaf epidermis have a specialized cuticle, and we investigate its function along with that of bulliform cells themselves. Bulliform cells displayed increased shrinkage compared to other epidermal cell types during dehydration of the leaf, providing a potential mechanism to facilitate leaf rolling. Analysis of natural variation was used to relate bulliform strip patterning to leaf rolling rate, providing further evidence of a role for bulliform cells in leaf rolling. Bulliform cell cuticles showed a distinct ultrastructure with increased cuticle thickness compared to other leaf epidermal cells. Comparisons of cuticular conductance between adaxial and abaxial leaf surfaces, and between bulliform‐enriched mutants versus wild‐type siblings, showed a correlation between elevated water loss rates and presence or increased density of bulliform cells, suggesting that bulliform cuticles are more water‐permeable. Biochemical analysis revealed altered cutin composition and increased cutin monomer content in bulliform‐enriched tissues. In particular, our findings suggest that an increase in 9,10‐epoxy‐18‐hydroxyoctadecanoic acid content, and a lower proportion of ferulate, are characteristics of bulliform cuticles. We hypothesize that elevated water permeability of the bulliform cell cuticle contributes to the differential shrinkage of these cells during leaf dehydration, thereby facilitating the function of bulliform cells in stress‐induced leaf rolling observed in grasses.
The leaf outer epidermal cell wall acts as a barrier against pathogen attack and desiccation, and as such is covered by a cuticle, composed of waxes and the polymer cutin. Cutin monomers are formed by the transfer of fatty acids to glycerol by glycerol‐3‐phosphate acyltransferases, which facilitate their transport to the surface. The extent to which cutin monomers affect leaf cell wall architecture and barrier properties is not known. We report a dual functionality of pathogen‐inducible Silencing of This study highlights a hitherto unknown role for GPAT6‐generated cutin monomers in influencing epidermal cell properties that are integral to leaf–microbe interactions and in limiting dehydration.
- NSF-PAR ID:
- 10385672
- Publisher / Repository:
- Wiley-Blackwell
- Date Published:
- Journal Name:
- New Phytologist
- Volume:
- 223
- Issue:
- 3
- ISSN:
- 0028-646X
- Format(s):
- Medium: X Size: p. 1547-1559
- Size(s):
- p. 1547-1559
- Sponsoring Org:
- National Science Foundation
More Like this
-
Abstract -
Summary Colonization by foliar endophytic fungi can affect the expression of host plant defenses and other ecologically important traits. However, whether endophyte colonization affects the uptake or redistribution of resources within and among host plant tissues remains unstudied.
We inoculated leaves of
Theobroma cacao with four common colonizers that range in their effect from protective to pathogenic (Colletotrichum tropicale ,Pestalotiopsis sp.,Colletotrichum theobromicola , orPhytophthora palmivora ). We pulsed the soil with nitrogen‐15 (15N) and then traced15N uptake and its subsequent distribution to whole plants and individual leaves.At a whole‐plant level,
C. tropicale ‐inoculated plants showed significantly greater15N uptake than endophyte‐free plants did in the same pot. Among leaves within plants, younger leaves were particularly enriched in15N, but endophyte inoculation at the individual leaf level did not alter15N distribution within plants. However, leaves co‐inoculated with pathogenicPhytophthora and protectiveC. tropicale experienced significantly elevated15N content as pathogen damage increased, compared with leaves inoculated only with the pathogen. Further, endophyte–pathogen co‐infection also increased total plant biomass.Our results indicate that colonization by foliar endophytes significantly affects N uptake and distribution among and within host plants in ways that appear to be context dependent on other microbiome components.
-
Summary Given increasing water deficits across numerous ecosystems world‐wide, it is urgent to understand the sequence of failure of leaf function during dehydration.
We assessed dehydration‐induced losses of rehydration capacity and maximum quantum yield of the photosystem
II (F v/F m) in the leaves of 10 diverse angiosperm species, and tested when these occurred relative to turgor loss, declines of stomatal conductanceg s, and hydraulic conductanceK leaf, including xylem and outside xylem pathways for the same study plants. We resolved the sequences of relative water content and leaf water potential Ψleafthresholds of functional impairment.On average, losses of leaf rehydration capacity occurred at dehydration beyond 50% declines of
g s,K leafand turgor loss point. Losses ofF v/F moccurred after much stronger dehydration and were not recovered with leaf rehydration. Across species, tissue dehydration thresholds were intercorrelated, suggesting trait co‐selection. Thresholds for each type of functional decline were much less variable across species in terms of relative water content than Ψleaf.The stomatal and leaf hydraulic systems show early functional declines before cell integrity is lost. Substantial damage to the photochemical apparatus occurs at extreme dehydration, after complete stomatal closure, and seems to be irreversible.
-
Summary All aerial epidermal cells in land plants are covered by the cuticle, an extracellular hydrophobic layer that provides protection against abiotic and biotic stresses and prevents organ fusion during development.
Genetic and morphological analysis of the classic maize
adherent1 (ad1 ) mutant was combined with genome‐wide binding analysis of the maize MYB transcription factor FUSED LEAVES1 (FDL1), coupled with transcriptional profiling offdl1 mutants.We show that
AD1 encodes an epidermally‐expressed 3‐KETOACYL‐CoA SYNTHASE (KCS) belonging to a functionally uncharacterized clade of KCS enzymes involved in cuticular wax biosynthesis. Wax analysis inad1 mutants indicates thatAD1 functions in the formation of very‐long‐chain wax components. We demonstrate that FDL1 directly binds to CCAACC core motifs present inAD1 regulatory regions to activate its expression. Over 2000 additional target genes of FDL1, including many involved in cuticle formation, drought response and cell wall organization, were also identified.Our results identify a regulatory module of cuticle biosynthesis in maize that is conserved across monocots and eudicots, and highlight previously undescribed factors in lipid metabolism, transport and signaling that coordinate organ development and cuticle formation.
-
Summary Isogenic individuals can display seemingly stochastic phenotypic differences, limiting the accuracy of genotype‐to‐phenotype predictions. The extent of this phenotypic variation depends in part on genetic background, raising questions about the genes involved in controlling stochastic phenotypic variation.
Focusing on early seedling traits in
Arabidopsis thaliana , we found that hypomorphs of the cuticle‐related geneLIPID TRANSFER PROTEIN 2 (LTP2 ) greatly increased variation in seedling phenotypes, including hypocotyl length, gravitropism and cuticle permeability. Manyltp2 hypocotyls were significantly shorter than wild‐type hypocotyls while others resembled the wild‐type.Differences in epidermal properties and gene expression between
ltp2 seedlings with long and short hypocotyls suggest a loss of cuticle integrity as the primary determinant of the observed phenotypic variation. We identified environmental conditions that reveal or mask the increased variation inltp2 hypomorphs and found that increased expression of its closest paralogLTP1 is necessary forltp2 phenotypes.Our results illustrate how decreased expression of a single gene can generate starkly increased phenotypic variation in isogenic individuals in response to an environmental challenge.