|
|
|
|
|
| Abscisic acid induces differential expression of genes involved in wound-induced suberization in postharvest tomato fruit |
| HAN Xue-yuan, MAO Lin-chun, LU Wen-jing, TAO Xiao-ya, WEI Xiao-peng, LUO Zi-sheng |
| College of Biosystems Engineering and Food Science/Fuli Institute of Food Science/Zhejiang Key Laboratory of AgroFood Processing, Zhejiang University, Hangzhou 310058, P.R.China |
|
|
|
|
Abstract Fruit wounding occurred at harvest and transportation requires rapid suberization as a major part of the healing process to prevent infection and desiccation. The focus of this work was to explore the mediation of abscisic acid (ABA) on wound-induced suberization and to determine expression profiles of specific genes involved in wound-induced suberization in tomato fruit. The measurements of weight loss and fruit firmness suggested wound-induced suberization started at 2 d after wounding. The suberization process with the accumulation of suberin polyphenolics (SPP) and polyaliphatics (SPA) observed through autofluorescence microscopy and Sudan IV staining was accelerated by ABA. Expressions of SlPAL5 and Sl4CL involved in the synthesis of SPP reached the highest at 4 and 8 d after wounding following ABA application, respectively. Associated with SPA biosynthesis, SlLACS1 and SlLACS2 showed the most abundant transcripts at 8 and 6 d in ABA group, respectively. Transcript levels including SlKCSs, SlCYP86B1, SlFAR3, and SlGPATs were up-regulated at 2 d after wounding by ABA. Activities of polyphenol oxidase and lipoxygenase were also enhanced during wound-induced suberization following ABA application. The results in this study proved that ABA accelerated the wound-induced suberization progress by increasing the transcript levels of relevant genes in postharvest tomato fruit.
|
|
Received: 05 January 2018
Accepted:
|
| Fund: This research was supported by the National Natural Science Foundation of China (31372113) and the National Basic Research Program of China (973 program, 2013CB127101). |
|
Corresponding Authors:
Correspondence MAO Lin-chun,E-mail: linchun@zju.edu.cn
|
| About author: HAN Xue-yun , Mobile: +86-18867146394, E-mail: 18867146394@163.com; |
Cite this article:
HAN Xue-yuan, MAO Lin-chun, LU Wen-jing, TAO Xiao-ya, WEI Xiao-peng, LUO Zi-sheng.
2018.
Abscisic acid induces differential expression of genes involved in wound-induced suberization in postharvest tomato fruit. Journal of Integrative Agriculture, 17(12): 2670-2682.
|
Aghdam M S, Asghari M, Khorsandi O, Mohayeji M. 2014. Alleviation of postharvest chilling injury of tomato fruit by salicylic acid treatment. Journal of Food Science and Technology, 51, 2815–2820.
Beisson F, Li Y, Bonaventure G, Pollard M, Ohlrogge J B. 2007. The acyltransferase GPAT5 is required for the synthesis of suberin in seed coat and root of Arabidopsis. The Plant Cell, 19, 351–368.
Bernards M A. 2002. Demystifying suberin. Canadian Journal of Botany, 80, 227–240.
Bernards M A, Summerhurst D K, Razem F A. 2004. Oxidases, peroxidases and hydrogen peroxide: The suberin connection. Phytochemistry Reviews: Proceedings of the Phytochemical Society of Europe, 3, 113–126.
Compagnon V, Diehl P, Benveniste I, Meyer D, Schaller H, Schreiber L, Franke R, Pinot F. 2009. CYP86B1 is required for very long chain ω-hydroxyacid and α, ω-dicarboxylic acid synthesis in root and seed suberin polyester. Plant Physiology, 150, 1831–1843.
Cookson S J, Moreno M J C, Hevin C, Mendome L Z N, Delrot S, Trossat-Magnin C, Ollat N. 2013. Graft union formation in grapevine induces transcriptional changes related to cell wall modification, wounding, hormone signalling, and secondary metabolism. Journal of Experimental Botany, 64, 2997–3008.
Dastmalchi K, Kallash L, Wang I, Phan V C, Huang W L, Serra O, Stark R E. 2015. Defensive armor of potato tubers: Nonpolar metabolite profiling, antioxidant assessment, and solid-state nmr compositional analysis of suberin-enriched wound-healing tissues. Journal of Agricultural and Food Chemistry, 63, 6810–6822.
Van Dijk C, Boeriu C, Peter F, Stolle-Smits T, Tijskens L M M. 2006. The firmness of stored tomatoes (cv. Tradiro). 1. Kinetic and near infrared models to describe firmness and moisture loss. Journal of Food Engineering, 77, 575–584.
Domergue F, Vishwanath S J, Joubès J, Ono J, Lee J A, Bourdon M, Alhattab R, Lowe C, Pascal S, Lessire R. 2010. Three Arabidopsis fatty acyl-coenzyme A reductases, FAR1, FAR4, and FAR5, generate primary fatty alcohols associated with suberin deposition. Plant Physiology, 153, 1539–1554.
Espelie K E, Kolattukudy P E. 1985. Purification and characterization of an abscisic acid-inducible anionic peroxidase associated with suberization in potato (Solanum tuberosum). Archives of Biochemistry and Biophysics, 240, 539–545.
Franke R, Höfer R, Briesen I, Emsermann M, Efremova N, Yephremov A, Schreiber L. 2009. The DAISY gene from Arabidopsis encodes a fatty acid elongase condensing enzyme involved in the biosynthesis of aliphatic suberin in roots and the chalaza-micropyle region of seeds. The Plant Journal, 57, 80–95.
Franke R B, Dombrink I, Schreiber L. 2012. Suberin goes genomics: Use of a short living plant to investigate a long lasting polymer. Frontiers in Plant Science, 3, 1–8.
Gardner H W. 1980. Lipid enzymes: Lipases, lipoxygenases, and “hydroperoxidases”. In: Autoxidation in Food and Biological Systems. Springer, USA. pp. 447–504.
Gill R, Gupta A, Taggar G, Taggar M. 2010. Review article: Role of oxidative enzymes in plant defenses against insect herbivory. Acta Phytopathologica et Entomologica Hungarica, 45, 277–290.
Hirt H. 1999. Transcriptional upregulation of signaling pathways: More complex than anticipated. Trends in Plant Science, 4, 7–8.
Isaacson T, Kosma D K, Matas A J, Buda G J, He Y, Yu B, Pravitasari A, Batteas J D, Stark R E, Jenks M A. 2009. Cutin deficiency in the tomato fruit cuticle consistently affects resistance to microbial infection and biomechanical properties, but not transpirational water loss. The Plant Journal, 60, 363–377.
Joos H J, Hahlbrock K. 1992. Phenylalanine ammonia-lyase in potato (Solanum tuberosum L.). European Journal of Biochemistry, 204, 621–629.
Kawahara Y, de la Bastide M, Hamilton J P, Kanamori H, McCombie W R, Ouyang S, Schwartz D C. 2013. Improvement of the Oryza sativa Nipponbare reference genome using next generation sequence and optical map data. Rice, 6, 4.
Kesanakurti D, Kolattukudy P E, Kirti P B. 2012. Fruit-specific overexpression of wound-induced tap1 under E8 promoter in tomato confers resistance to fungal pathogens at ripening stage. Physiologia Plantarum, 146, 136–148.
Kolattukudy P E. 2001. Polyesters in higher plants. In: Biopolyesters. Springer, USA. pp. 1–49.
Kumar G M, Lulai E C, Suttle J C, Knowles N R. 2010. Age-induced loss of wound-healing ability in potato tubers is partly regulated by ABA. Planta, 232, 1433–1445.
Lashbrooke J, Aharoni A, Costa F. 2015. Genome investigation suggests MdSHN3, an APETALA2-domain transcription factor gene, to be a positive regulator of apple fruit cuticle formation and an inhibitor of russet development. Journal of Experimental Botany, 66, 6579–6589.
Lashbrooke J, Cohen H, Levy-Samocha D, Tzfadia O, Panizel I, Zeisler V, Massalha H, Stern A, Trainotti L, Schreiber L, Costa F, Aharoni A. 2016. MYB107 and MYB9 homologs regulate suberin deposition in angiosperms. The Plant Cell, 28, 2097–2116.
Lee S B, Jung S J, Go Y S, Kim H U, Kim J K, Cho H J, Park O K, Suh M C. 2009. Two Arabidopsis 3-ketoacyl CoA synthase genes, KCS20 and KCS2/DAISY, are functionally redundant in cuticular wax and root suberin biosynthesis, but differentially controlled by osmotic stress. The Plant Journal, 60, 462–475.
Lendzian K J. 2006. Survival strategies of plants during secondary growth: Barrier properties of phellems and lenticels towards water, oxygen, and carbon dioxide. Journal of Experimental Botany, 57, 2535–2546.
Lewis N G, Davin L B, Sarkanen S, Pinto B M. 1999. The nature and function of lignins. Comprehensive Natural Products Chemistry, 3, 617–745.
Li-Beisson Y, Shorrosh B, Beisson F, Andersson M X, Arondel V, Bates P D, Baud S, Bird D, DeBono A, Durrett T P. 2013. Acyl-lipid metabolism. The Arabidopsis Book, 8, e0161.
Li Y, Beisson F, Koo A J, Molina I, Pollard M, Ohlrogge J. 2007. Identification of acyltransferases required for cutin biosynthesis and production of cutin with suberin-like monomers. Proceedings of the National Academy of Sciences of the United States of America, 104, 18339–18344.
Liu J, Tian S P, Meng X H, Xu Y. 2007. Effects of chitosan on control of postharvest diseases and physiological responses of tomato fruit. Postharvest Biology and Technology, 44, 300–306.
Livak K J, Schmittgen D. 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2–??CT method. Methods, 25, 402–408.
Lozano-Baena M D, Prats E, Moreno M T, Rubiales D, Perez-de-Luque A. 2007. Medicago truncatula as a model for nonhost resistance in legume-parasitic plant interactions. Plant Physiology, 145, 437–449.
Lu S Y, Song T, Kosma D K, Parsons E P, Rowland O, Jenks M A. 2009. Arabidopsis CER8 encodes long-chain acyl-CoA synthetasee 1 (LACS1) that has overlapping functions with LACS2 in plant wax and cutin synthesis. The Plant Journal, 59, 553–564.
Lucena M A, Romero-Aranda R, Mercado J A, Cuartero J, Valpuesta V, Quesada M A. 2003. Structural and physiological changes in the roots of tomato plants over-expressing a basic peroxidase. Physiologia Plantarum, 118, 422–429.
Lulai E C, Neubauer J D. 2014. Wound-induced suberization genes are differentially expressed, spatially and temporally, during closing layer and wound periderm formation. Postharvest Biology and Technology, 90, 24–33.
Lulai E C, Suttle J C, Pederson S M. 2008. Regulatory involvement of abscisic acid in potato tuber wound-healing. Journal of Experimental Botany, 59, 1175–1186.
Mintz-Oron S, Mandel T, Rogachev I, Feldberg L, Lotan O, Yativ M, Wang Z, Jetter R, Venger I, Adato A, Aharoni A. 2008. Gene expression and metabolism in tomato fruit surface tissues. Plant Physiology, 147, 823–851.
Molina I, Li-Beisson Y, Beisson F, Ohlrogge J B, Pollard M. 2009. Identification of an Arabidopsis feruloyl-coenzyme A transferase required for suberin synthesis. Plant Physiology, 151, 1317–1328.
Paul S, Gable K, Beaudoin F, Cahoon E, Jaworski J, Napier J A, Dunn T M. 2006. Members of the Arabidopsis FAE1-like 3-ketoacyl-CoA synthase gene family substitute for the Elop proteins of Saccharomyces cerevisiae. The Journal of Biological Chemistry, 281, 9018–9029.
Petit J, Bres C, Mauxion J P, Tai F W J, Martin L B, Fich E A, Joubès J, Rose J K, Domergue F, Rothan C. 2016. The glycerol-3-phosphate acyltransferase GPAT6 from tomato plays a central role in fruit cutin biosynthesis. Plant Physiology, 171, 894–913.
Pollard M, Beisson F, Li Y, Ohlrogge J B. 2008. Building lipid barriers: Biosynthesis of cutin and suberin. Trends in Plant Science, 13, 236–246.
Quiroga M, Forchetti S M, Taleisnik E, Tigier H A. 2001. Tomato root peroxidase isoenzymes: Kinetic studies of the coniferyl alcohol peroxidase activity, immunological properties and role in response to salt stress. Journal of Plant Physiology, 158, 1007–1013.
Quiroga M, Guerrero C, Botella M A, Barceló A, Amaya I, Medina M I, Alonso F J, Silvia Milrad de F, Tigier H, Valpuesta V. 2000. A tomato peroxidase involved in the synthesis of lignin and suberin. Plant Physiology, 122, 1119–1127.
Ranathunge K, Schreiber L, Franke R. 2011. Suberin research in the genomics era-new interest for an old polymer. Plant Science: An International Journal of Experimental Plant Biology, 180, 399–413.
Razem F A, Bernards M A. 2003. Reactive oxygen species production in association with suberization: Evidence for an NADPH-dependent oxidase. Journal of Experimental Botany, 54, 935–941.
Rhodes J M, Wooltorton L S C. 1978. The biosynthesis of phenolic compounds in wounded plant storage tissues. Biochemistry of Wounded Plant Tissues, 243–286.
Rowland O, Domergue F. 2012. Plant fatty acyl reductases: enzymes generating fatty alcohols for protective layers with potential for industrial applications. Plant Science: An International Journal of Experimental Plant Biology, 193, 28–38.
Schnurr J, Shockey J. 2004. The acyl-CoA synthetase encoded by LACS2 is essential for normal cuticle development in Arabidopsis. The Plant Cell, 16, 629–642.
Schreiber L, Franke R, Hartmann K D, Ranathunge K, Steudle E. 2005. The chemical composition of suberin in apoplastic barriers affects radial hydraulic conductivity differently in the roots of rice (Oryza sativa L. cv. IR64) and corn (Zea mays L. cv. Helix). Journal of Experimental Botany, 56, 1427–1436.
Serra O, Soler M, Hohn C, Franke R, Schreiber L, Prat S, Molinas M, Figueras M. 2009. Silencing of StKCS6 in potato periderm leads to reduced chain lengths of suberin and wax compounds and increased peridermal transpiration. Journal of Experimental Botany, 60, 697–707.
Soler M, Serra O, Molinas M, Huguet G, Fluch S, Figueras M. 2007. A genomic approach to suberin biosynthesis and cork differentiation. Plant Physiology, 144, 419–431.
Subramanian N, Venkatesh P, Ganguli S, Sinkar V P. 1999. Role of polyphenol oxidase and peroxidase in the generation of black tea theaflavins. Journal of Agricultural and Food Chemistry, 47, 2571–2578.
Suttle J C, Lulai E C, Huckle L L, Neubauer J D. 2013. Wounding of potato tubers induces increases in ABA biosynthesis and catabolism and alters expression of ABA metabolic genes. Journal of Plant Physiology, 170, 560–566.
Tao X Y, Mao L C, Li J Y, Chen J X, Lu W J, Huang S. 2016. Abscisic acid mediates wound-healing in harvested tomato fruit. Postharvest Biology and Technology, 118, 128–133.
Tenhaken R, Levine A, Brisson L F, Dixon R A, Lamb C. 1995. Function of the oxidative burst in hypersensitive disease resistance. Proceedings of the National Academy of Sciences of the United States of America, 92, 4158–4163.
Vishwanath S J, Delude C, Domergue F, Rowland O. 2015. Suberin: Biosynthesis, regulation, and polymer assembly of a protective extracellular barrier. Plant Cell Reports, 34, 573–586.
Wang Y, Wang M L, Sun Y L, Wang Y T, Li T T, Chai G Q, Jiang W H, Shan L W, Li C L, Xiao E S, Wang Z H. 2015. FAR5, a fatty acyl-coenzyme A reductase, is involved in primary alcohol biosynthesis of the leaf blade cuticular wax in wheat (Triticum aestivum L.). Journal of Experimental Botany, 66, 1165–1178.
Whetten R W, MacKay J J, Sederoff R R. 1998. Recent advances in understanding lignin biosynthesis. Annual Review of Plant Physiology and Plant Molecular Biology, 49, 585–609.
Yang W, Pollard M, Li-Beisson Y, Beisson F, Feig M, Ohlrogge J. 2010. A distinct type of glycerol-3-phosphate acyltransferase with sn-2 preference and phosphatase activity producing 2-monoacylglycerol. Proceedings of the National Academy of Sciences of the United States of America, 107, 12040–12045.
|
| No Suggested Reading articles found! |
|
|
Viewed |
|
|
|
Full text
|
|
|
|
|
Abstract
|
|
|
|
|
Cited |
|
|
|
|
| |
Shared |
|
|
|
|
| |
Discussed |
|
|
|
|
