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

Haoliang Wan , Hongbo Liu , Jingyu Zhang , Yi Lyu , Zhuoran Li , Yizhong He , Xiaoliang Zhang , Xiuxin Deng , Yariv Brotman , Alisdair R. Fernie , Yunjiang Cheng , Weiwei Wen

Horticulture Research ›› 2020, Vol. 7 ›› Issue (1) : 41

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Horticulture Research ›› 2020, Vol. 7 ›› Issue (1) :41 DOI: 10.1038/s41438-020-0262-z
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Lipidomic and transcriptomic analysis reveals reallocation of carbon flux from cuticular wax into plastid membrane lipids in a glossy “Newhall” navel orange mutant
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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, time-resolved 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.

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Haoliang Wan, Hongbo Liu, Jingyu Zhang, Yi Lyu, Zhuoran Li, Yizhong He, Xiaoliang Zhang, Xiuxin Deng, Yariv Brotman, Alisdair R. Fernie, Yunjiang Cheng, Weiwei Wen. Lipidomic and transcriptomic analysis reveals reallocation of carbon flux from cuticular wax into plastid membrane lipids in a glossy “Newhall” navel orange mutant. Horticulture Research, 2020, 7 (1) : 41 DOI:10.1038/s41438-020-0262-z

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References

[1]

Ben-Yehoshua, S., Burg, S. P. & Young, R. Resistance of citrus fruit to mass transport of water vapor and other gases. Plant Physiol. 79, 1048-1053 (1985).

[2]

El-Otmani, M., Coggins Jr, C. & Eaks, I. Fruit age and gibberellic acid effect on epicuticular wax accumulation, respiration, and internal atmosphere of navel orange fruit. J. Am. Soc. Hortic. Sci. 111, 228-232 (1986).

[3]

Liu, D. C. et al. A comparison of the ultrastructure and composition of fruits’ cuticular wax from the wild-type ‘Newhall’ navel orange (Citrus sinensis [L.] Osbeck cv. Newhall) and its glossy mutant. Plant Cell Rep. 31, 2239-2246 (2012).

[4]

He, Y. et al. Integrated transcriptomic and metabolomic analyses of a wax deficient citrus mutant exhibiting jasmonic acid-mediated defense against fungal pathogens. Hortic. Res. 5, 43 (2018).

[5]

Hadley, N. F. Lipid water barriers in biological systems. Prog. Lipid Res. 28, 1-33 (1989).

[6]

Boudiere, L. et al. Glycerolipids in photosynthesis: composition, synthesis and trafficking. Biochim. Biophys. Acta 1837, 470-480 (2014).

[7]

Hurlock, A. K., Roston, R. L., Wang, K. & Benning, C. Lipid trafficking in plant cells. Traffic 15, 915-932 (2014).

[8]

Voisin, D. et al. Dissection of the complex phenotype in cuticular mutants of Arabidopsis reveals a role of SERRATE as a mediator. PLoS Genet. 5, e1000703 (2009).

[9]

Kunst, L. & Samuels, A. L. Biosynthesis and secretion of plant cuticular wax. Prog. Lipid Res. 42, 51-80 (2003).

[10]

Gustavo, B., Xiaoming, B., John, O. & Mike, P. Metabolic responses to the reduction in palmitate caused by disruption of the FATB gene in Arabidopsis. Plant Physiol. 135, 1269-1279 (2004).

[11]

Jones, M. R. Lipids in photosynthetic reaction centres: Structural roles and functional holes. Prog. Lipid Res. 46, 56-87 (2007).

[12]

Fujii, S., Kobayashi, K., Nagata, N., Masuda, T. & Wada, H. Monogalactosyldiacylglycerol facilitates synthesis of photoactive protochlorophyllide in etioplasts. Plant Physiol. 174, 2183-2198 (2017).

[13]

Zhang, M. et al. Modulated fatty acid desaturation via overexpression of two distinct omega-3 desaturases differentially alters tolerance to various abiotic stresses in transgenic tobacco cells and plants. Plant J. 44, 361-371 (2010).

[14]

Liu, X. Y. et al. Overexpression of tomato chloroplast omega-3 fatty acid desaturase gene alleviates the photoinhibition of photosystems 2 and 1 under chilling stress. Photosynthetica 46, 185-192 (2008).

[15]

Moellering, E. R. & Benning, C. Galactoglycerolipid metabolism under stress: a time for remodeling. Trends Plant Sci. 16, 98-107 (2011).

[16]

Ryu, S. B. Phospholipid-derived signaling mediated by phospholipase A in plants. Trends Plant Sci. 9, 229-235 (2004).

[17]

Richmond, G. S. & Smith, T. K. Phospholipases, A1. Int. J. Mol. Sci. 12, 588-612 (2011).

[18]

Ellinger, D. et al. DONGLE and DEFECTIVE IN ANTHER DEHISCENCE1 lipases are not essential for wound- and pathogen-induced jasmonate biosynthesis: redundant lipases contribute to jasmonate formation. Plant Physiol. 153, 114-127 (2010).

[19]

Wasternack, C. H. B. Jasmonates: biosynthesis, perception, signal transduction and action in plant stress response, growth and development. An update to the 2007 review in Annals of Botany. Ann. Bot. 111, 1021-1058 (2013).

[20]

Wang, K. et al. Two abscisic acid-responsive plastid lipase genes involved in jasmonic acid biosynthesis in Arabidopsis thaliana. Plant Cell 30, 1006-1022 (2018).

[21]

Christeller, J. T. & Galis, I. alpha-linolenic acid concentration and not wounding per se is the key regulator of octadecanoid (oxylipin) pathway activity in rice (Oryza sativa L.) leaves. Plant Physiol. Biochem. 83, 117-125 (2014).

[22]

Wang, J. et al. Regulation of cuticle formation during fruit development and ripening in ‘Newhall’ navel orange (Citrus sinensis Osbeck) revealed by transcriptomic and metabolomic profiling. Plant Sci.: Int. J. Exp. Plant Biol. 243, 131-144 (2016).

[23]

Wang, J. et al. Comparative analysis of surface wax in mature fruits between Satsuma mandarin (Citrus unshiu) and ‘Newhall’ navel orange (Citrus sinensis) from the perspective of crystal morphology, chemical composition and key gene expression. Food Chem. 153, 177-185 (2014).

[24]

Li-Beisson, Y. et al. Acyl-lipid metabolism. Arabidopsis Book 11, e0161. https://doi.org/10.1199/tab.016110.1199/tab.0133 (2013).

[25]

Liu, D. et al. Transcriptome sequencing identified wax-related genes controlling the glossy phenotype formation of “Ganqi 3,” a bud mutant derived from wild-type “Newhall” navel orange. Tree Genet. Genom. 12, https://doi.org/10.1007/s11295-016-1017-8 (2016).

[26]

Ohlrogge, J. & Browse, J. Lipid biosynthesis. Plant Cell 7, 957 (1995).

[27]

Fabre, G. et al. The ABCG transporter PEC1/ABCG32 is required for the formation of the developing leaf cuticle in Arabidopsis. New Phytologist 209, 192-201 (2016).

[28]

Li, L. et al. The maize glossy13 gene, cloned via BSR-Seq and Seq-walking encodes a putative ABC transporter required for the normal accumulation of epicuticular waxes. PLoS ONE 8, e82333 (2013).

[29]

David, P. et al. The Arabidopsis DESPERADO/AtWBC11 transporter is required for cutin and wax secretion. Plant Physiol. 145, 1345-1360 (2007).

[30]

Xu, C., Fan, J., Froehlich, J. E., Awai, K. & Benning, C. Mutation of the TGD1 chloroplast envelope protein affects phosphatidate metabolism in Arabidopsis. Plant Cell 17, 3094-3110 (2005).

[31]

Gimenez-Ibanez, S. et al. JAZ2 controls stomata dynamics during bacterial invasion. New Phytologist 213, 1378-1392 (2017).

[32]

Seo, Y. S., Kim, E. Y., Kim, J. H. & Kim, W. T. Enzymatic characterization of class I DAD1-like acylhydrolase members targeted to chloroplast in Arabidopsis. FEBS Lett. 583, 2301-2307 (2009).

[33]

Wood, C. C. et al. A leaf-based assay using interchangeable design principles to rapidly assemble multistep recombinant pathways. Plant Biotechnol. J. 7, 914-924 (2009).

[34]

Dussert, S. et al. Comparative transcriptome analysis of three oil palm fruit and seed tissues that differ in oil content and fatty acid composition. Plant Physiol. 162, 1337-1358 (2013).

[35]

Yang, D.-H., Hettenhausen, C., Baldwin, I. T. & Wu, J. Silencing Nicotiana attenuata calcium-dependent protein kinases, CDPK4 and CDPK5, strongly up-regulates wound-and herbivory-induced jasmonic acid accumulations. Plant Physiol. 159, 1591-1607 (2012).

[36]

Jetter, R. & Kunst, L. Plant surface lipid biosynthetic pathways and their utility for metabolic engineering of waxes and hydrocarbon biofuels. Plant J. 54, 670-683 (2008).

[37]

Kimbara, J. et al. Inhibition of CUTIN DEFICIENT 2 causes defects in cuticle function and structure and metabolite changes in tomato fruit. Plant Cell Physiol. 54, 1535-1548 (2013).

[38]

Xia, Y. et al. The glabra1 mutation affects cuticle formation and plant responses to microbes. Plant Physiol. 154, 833-846 (2010).

[39]

Xia, Y. et al. An intact cuticle in distal tissues is essential for the induction of systemic acquired resistance in plants. Cell Host Microbe 5, 151-165 (2009).

[40]

Gao, Q.-M. Glycerolipids and the Plant Cuticle Contribute to Plant Immunity. Theses and Dissertations-Plant Pathology. 4, https://uknowledge.uky.edu/plantpath_etds/4 (2012).

[41]

Xia, Y. The Role of Cuticle, Fatty Acids, and Lipid Signaling in Plant Defense. Theses and Dissertations-Plant Pathology. 10, https://uknowledge.uky.edu/plantpath_etds/10 (2010).

[42]

Pighin, J. A. et al. Plant cuticular lipid export requires an ABC transporter. Science 306, 702 (2004).

[43]

Park, C. S., Go, Y. S. & Suh, M. C. Cuticular wax biosynthesis is positively regulated by WRINKLED 4, an AP 2/ERF‐type transcription factor, in Arabidopsis stems. Plant J. 88, 257-270 (2016).

[44]

Li, Q. et al. Understanding the biochemical basis of temperature-induced lipid pathway adjustments in plants. Plant Cell 27, 86-103 (2015).

[45]

Hugly, S., Kunst, L. & Somerville, C . Enhanced thermal tolerance of photosynthesis and altered chloroplast ultrastructure in a mutant of Arabidopsis deficient in lipid desaturation. Plant Physiol. 90, 1134-1142 (1989).

[46]

Stintzi, A., Weber, H., Reymond, P. & Farmer, E. E. Plant defense in the absence of jasmonic acid: the role of cyclopentenones. Proc. Natl Acad. Sci. USA 98, 12837-12842 (2001).

[47]

Bonaventure, G., Salas, J. J., Pollard, M. R. & Ohlrogge, J. B. Disruption of the FATB gene in Arabidopsis demonstrates an essential role of saturated fatty acids in plant growth. Plant Cell 15, 1020 (2003).

[48]

Lim, G. H., Singhal, R., Kachroo, A. & Kachroo, P. Fatty acid- and lipid-mediated signaling in plant defense. Annu. Rev. Phytopathol. 55, 505 (2017).

[49]

Hyun, Y. et al. Cooperation and functional diversification of two closely related galactolipase genes for jasmonate biosynthesis. Dev. Cell 14, 183-192 (2008).

[50]

Lu, S., Liu, H., Jin, C., Li, Q. & Guo, L. An efficient and comprehensive plant glycerolipids analysis approach based on high‐performance liquid chromatography-quadrupole time‐of‐flight mass spectrometer. Plant Direct 3, e00183 (2019).

[51]

Liu, H., Li, X., Xiao, J. & Wang, S. A convenient method for simultaneous quantification of multiple phytohormones and metabolites: application in study of rice-bacterium interaction. Plant Methods 8, 2 (2012).

[52]

Liu, Y. Z., Liu, Q. & Tao, N. G. Efficient isolation of RNA from fruit peel and pulp of ripening navel orange (Citrus sinensis Osbeck). J. Huazhong Agric. Univ. 25, 300-304 (2006).

[53]

Xu, Q. et al. The draft genome of sweet orange (Citrus sinensis). Nat. Genet. 45, 59-66 (2013).

[54]

Bustin, S. A. et al. The MIQE guidelines: minimum information for publication of quantitative real-time PCR experiments. Clin. Chem. 55, 611-622 (2009).

[55]

Xie, C. et al. KOBAS 2.0: a web server for annotation and identification of enriched pathways and diseases. Nucleic Acids Res. 39, W316-W322 (2011).

[56]

Yoo, S.-D., Cho, Y.-H. & Sheen, J. Arabidopsis mesophyll protoplasts: a versatile cell system for transient gene expression analysis. Nat. Protoc. 2, 1565 (2007).

[57]

Olivier, V., Susana, R., Pere, M. & David, B. An enhanced transient expression system in plants based on suppression of gene silencing by the p19 protein of tomato bushy stunt virus. Plant J. 33, 949-956 (2010).

[58]

Sparkes, I. A., Runions, J., Kearns, A. & Hawes, C. Rapid, transient expression of fluorescent fusion proteins in tobacco plants and generation of stably transformed plants. Nat. Protoc. 1, 2019-2025 (2006).

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