Genetic and environmental variation impact the cuticular hydrocarbon metabolome on the stigmatic surfaces of maize

Abstract

Background Simple non-isoprenoid hydrocarbons accumulate in discrete regions of the biosphere, including within bacteria and algae as a carbon and/or energy store, and the cuticles of plants and insects, where they may protect against environmental stresses. The extracellular cuticular surfaces of the stigmatic silks of maize are rich in linear hydrocarbons and therefore provide a convenient system to study the biological origins and functions of these unique metabolites. Results To test the hypotheses that genetics and environment influence the accumulation of surface hydrocarbons on silks and to examine the breadth of metabolome compositions across diverse germplasm, cuticular hydrocarbons were analyzed on husk-encased silks and silks that emerged from the husk leaves from 32 genetically diverse maize inbred lines, most of which are commonly utilized in genetics experiments. Total hydrocarbon accumulation varied ~ 10-fold among inbred lines, and up to 5-fold between emerged and husk-encased silks. Alkenes accounted for 5-60% of the total hydrocarbon metabolome, and the majority of alkenes were monoenes with a double bond at either the 7th or 9th carbon atom of the alkyl chain. Total hydrocarbon accumulation was impacted to similar degrees by genotype and husk encasement status, whereas genotype predominantly impacted alkene composition. Only minor differences in the metabolome were observed on silks that were emerged into the external environment for 3- versus 6-days. The environmental influence on the metabolome was further investigated by growing inbred lines in 2 years, one of which was warmer and wetter. Inbred lines grown in the drier year accumulated up to 2-fold more hydrocarbons and up to a 22% higher relative abundance of alkenes. In summary, the surface hydrocarbon metabolome of silks is primarily governed by genotype and husk encasement status, with smaller impacts of environment and genotype-by-environment interactions. Conclusions This study reveals that the composition of the cuticular hydrocarbon metabolome on silks is affected significantly by genetic factors, and is therefore amenable to dissection using quantitative genetic approaches. Such studies will clarify the genetic mechanisms responsible for the accumulation of these metabolites, enabling detailed functional investigations of the diverse and complex protective roles of silk surface lipids against environmental stresses.

Dynamic product-precursor relationships underlie cuticular lipid accumulation on maize silks

“…For example, in maize, the cuticular lipids on juvenile and adult leaves are primarily composed of alcohols, aldehydes and esters, with only about 1% and 17% being hydrocarbons, respectively (Bianchi et al, 1984; Bianchi et al, 1985). In contrast, for maize silks, which are the stigmatic floral tissues that receive pollen and facilitate fertilization of the ovule, cuticular lipids are particularly rich in hydrocarbons, comprising 40-90% of these lipids, with only minor amounts of VLCFAs, aldehydes and alcohols (Yang et al, 1992; Perera et al, 2010; Loneman et al, 2017; Dennison et al, 2019).…”

“…However, if the process begins with odd-numbered VLCFAs (i.e., 2n + 1 carbons), then even-numbered hydrocarbon products are produced (i.e., (2n + 1) – 1 = 2n ). Such even-numbered hydrocarbons occur in many cuticles, including that of maize silks (Yang et al, 1992; Loneman et al, 2017; Dennison et al, 2019). This sequence of hydrocarbon-forming reactions can occur in parallel at each VLCFA-CoA chain length (i.e., at every value of n ), thereby generating a homologous series of cuticular hydrocarbon products with alkyl chain lengths ranging from 19-33 carbon atoms.…”

“…Indeed, both genetic and environmental factors impact the cuticular lipid metabolome on maize silks. For example, multiple characterizations of the maize silk cuticular lipid metabolome revealed substantial differences (i.e., up to 10-fold) in lipid abundance among various panels of inbred genotypes, demonstrating the breadth of natural variation in cuticular composition (Miller et al, 2003; Perera et al, 2010; Loneman et al, 2017; Dennison et al, 2019). Moreover, within any individual maize inbred line, cuticular lipid accumulation varies along the length of the silks.…”

A multigenotype maize silk expression atlas reveals how exposure‐related stresses are mitigated following emergence from husk leaves

“…Indeed, silks exhibit a high level of phenotypic variability in emergence rates across diverse germplasm under drought (Bolaños & Edmeades, 1996), as well as differences in susceptibility to different pathogens (Lübberstedt, Klein, & Melchinger, 1998) and pests (Abel, Wilson, Wiseman, White, & Davis, 2000;Lopez et al, 2019). Moreover, the composition of many specialized metabolites varies among cultivars, including maysin (Byrne et al, 1996;Szalma, Buckler, Snook, & McMullen, 2005) and cuticular lipids (Dennison et al, 2019;Loneman et al, 2017;Perera et al, 2010). The emergence of plant tissues, such as during seedling emergence from the ground or monocot leaf emergence from a whorl, introduces microenvironmental changes and therefore new stresses.…”

Maize Glossy2 and Glossy2-like Genes Have Overlapping and Distinct Functions in Cuticular Lipid Deposition

“…Specifically, in juvenile leaves of maize seedlings, the reductive pathway predominates, and the expression of this metabolic network is under the control of the juvenile-to-adult phase transition, mediated by the transcription factor Gl15 (Moose and Sisco, 1996). By contrast, the fatty acid elongation-decarbonylative pathway is primarily expressed in silks (Perera et al, 2010;Loneman et al, 2017;Dennison et al, 2019). The gl mutations that have been characterized since the early-1900s have been identified via phenotypic screens of seedling leaves (Hayes and Brewbaker, 1928), which therefore primarily affect the fatty acid elongation-reductive pathway.…”