Lipidomic and transcriptomic analysis reveals reallocation of carbon flux from cuticular wax into plastid membrane lipids in a glossy “Newhall” navel orange mutant

Abstract

Both cuticle and membrane lipids play essential roles in quality maintenance and disease resistance in fresh fruits. Many reports have indicated the modification of alternative branch pathways in epicuticular wax mutants; however, the specific alterations concerning lipids have not been clarified thus far. Here, we conducted a comprehensive, timeresolved lipidomic, and transcriptomic analysis on the "Newhall" navel orange (WT) and its glossy mutant (MT) "Gannan No. 1". The results revealed severely suppressed wax formation accompanied by significantly elevated production of 36-carbon plastid lipids with increasing fruit maturation in MT. Transcriptomics analysis further identified a series of key functional enzymes and transcription factors putatively involved in the biosynthesis pathways of wax and membrane lipids. Moreover, the high accumulation of jasmonic acid (JA) in MT was possibly due to the need to maintain plastid lipid homeostasis, as the expression levels of two significantly upregulated lipases (CsDAD1 and CsDALL2) were positively correlated with plastid lipids and characterized to hydrolyze plastid lipids to increase the JA content. Our results will provide new insights into the molecular mechanisms underlying the natural variation of plant lipids to lay a foundation for the quality improvement of citrus fruit.

Update on Cuticular Wax Biosynthesis and Its Roles in Plant Disease Resistance

“…As the outmost layer exposed to the environment, cuticle covers plant aerial organs and protects plant tissues against enormous environmental challenges such as dehydration, excessive UV radiation, mechanical damage, and even pathogen infections, which have been summarized in prior reviews [ 30 , 31 , 32 , 33 , 34 , 35 , 36 , 37 , 38 , 39 , 40 , 41 , 42 , 43 , 44 , 45 ]. In addition to its protective roles, cuticle also gets involved in regulating plant development [ 33 ].…”

Function and transcriptional regulation of CsKCS20 in the elongation of very-long-chain fatty acids and wax biosynthesis in Citrus sinensis flavedo

“…Considering that β-ketoacyl-CoA synthase (KCS) is the rate-limiting enzyme in the VLCFA elongation process and determines the carbon chain distribution of wax components, we first analyzed the expression of all 16 KCS family genes based on previous transcriptome data [ 32 ] ( Supplementary Fig. S1 ).…”

“…However, the high heterozygosity, long juvenile phase and difficulty in transgenic processes have largely hindered the validation of such regulatory mechanisms, and there are only a limited number of reports on the biosynthesis of anthocyanins and carotenoids based on natural mutants [ 29 – 31 ]. Over the past decade, although several glossy citrus mutants have been analyzed by integrated transcriptome and metabolome analysis, the findings are mainly focused on the description of wax-deficient phenotypes, influence on plastid membrane lipids and defense against fungal pathogens [ 15 , 32 , 33 ]. In this study, by comparing “Newhall” navel orange (WT) with its glossy mutant (MT), in which the elongation of VLC acyl-CoAs above C 20 is blocked, we identified a wax biosynthesis enzyme, CsKCS20, which can catalyze the elongation process to form C 22 and C 24 VLCFAs and plays important roles in carbon chain distribution and cuticular wax biosynthesis in citrus fruit.…”

Metabolic Profiling and Gene Expression Analysis Unveil Differences in Flavonoid and Lipid Metabolisms Between ‘Huapi’ Kumquat (Fortunella crassifolia Swingle) and Its Wild Type

“…Recently, studies on the glossy surface of the ‘Newhall’ navel orange mutant demonstrated that the decrease in aliphatic wax components such as aldehydes, alkanes, alcohols, and fatty acids was related to its glossy phenotype ( Liu et al, 2015 ; He et al, 2019 ). Another study found that the plastid lipids (including monogalactosyldiacylglycerols, digalactosyldiacylglycerols, and lysophosphatidylglycerols) and the phospholipid precursors (including phosphatidic acids and DAGs) were highly accumulated in the glossy mutant ( Wan et al, 2020 ). Although HP fruit possessed glossy peel, it showed a decrease in the lipids, particularly the LysoPCs and LysoPEs in the peel and flesh, compared with those in RA fruit.…”