Wounding induces suberin deposition, relevant gene expressions and changes of endogenous phytohormones in Chinese yam (Dioscorea opposita) tubers
Linyao Liu
A , Ping Geng B , Xueyuan Jin C , Xiaopeng Wei A * , Jing Xue A , Xiaobo Wei D , Lihua Zhang A , Mengpei Liu A , Liang Zhang E , Wei Zong A and Linchun Mao F *
+ Author Affiliations
- Author Affiliations
A College of Food and Bioengineering, Zhengzhou University of Light Industry, Zhengzhou, Henan 450002, China.
B College of Energy and Power Engineering, Zhengzhou University of Light Industry, Zhengzhou, Henan 450002, China.
C College of Clinical Medicine, Hainan Vocational University of Science and Technology, Haikou, Hainan 571126, China.
D School of Food and Wine, Ningxia University, Ningxia Key Laboratory for Food Microbial-Applications Technology and Safety Control, Yinchuan, 750021, China.
E Wencheng Institution of Modern Agriculture and Healthcare Industry, Wenzhou 325300, China.
F College of Biosystems Engineering and Food Science, Zhejiang Key Laboratory of Agro-Food Processing, Zhejiang R&D Center of Food Technology and Equipment, Fuli Institute of Food Science, Zhejiang University, Hangzhou 310058, China.
Functional Plant Biology 50(9) 691-700 https://doi.org/10.1071/FP22280
Submitted: 16 November 2022 Accepted: 19 June 2023 Published: 13 July 2023
© 2023 The Author(s) (or their employer(s)). Published by CSIRO Publishing
Abstract
Wounds on Chinese yam (Dioscorea opposita) tubers can ocurr during harvest and handling, and rapid suberisation of the wound is required to prevent pathogenic infection and desiccation. However, little is known about the causal relationship among suberin deposition, relevant gene expressions and endogenous phytohormones levels in response to wounding. In this study, the effect of wounding on phytohormones levels and the expression profiles of specific genes involved in wound-induced suberisation were determined. Wounding rapidly increased the expression levels of genes, including PAL, C4H, 4CL, POD, KCSs, FARs, CYP86A1, CYP86B1, GPATs, ABCGs and GELPs, which likely involved in the biosynthesis, transport and polymerisation of suberin monomers, ultimately leading to suberin deposition. Wounding induced phenolics biosynthesis and being polymerised into suberin poly(phenolics) (SPP) in advance of suberin poly(aliphatics) (SPA) accumulation. Specifically, rapid expression of genes (e.g. PAL, C4H, 4CL, POD) associated with the biosynthesis and polymerisation of phenolics, in consistent with SPP accumulation 3 days after wounding, followed by the massive accumulation of SPA and relevant gene expressions (e.g. KCSs, FARs, CYP86A1/B1, GPATs, ABCGs, GELPs). Additionally, wound-induced abscisic acid (ABA) and jasmonic acid (JA) consistently correlated with suberin deposition and relevant gene expressions indicating that they might play a central role in regulating wound suberisation in yam tubers.
Keywords: abscisic acid, Chinese yam tuber, deposition, jasmonic acid, suberin poly(aliphatics), suberin poly(phenolics), suberisation and wound healing.
References
Arrietabaez D, Stark RE (2006) Modeling suberization with peroxidase-catalyzed polymerization of hydroxycinnamic acids: cross-coupling and dimerization reactions. Phytochemistry 67, 743–753.| Modeling suberization with peroxidase-catalyzed polymerization of hydroxycinnamic acids: cross-coupling and dimerization reactions.Crossref | GoogleScholarGoogle Scholar |
Beisson F, Li Y, Bonaventure G, Pollard M, Ohlrogge JB (2007) The acyltransferase GPAT5 is required for the synthesis of suberin in seed coat and root of Arabidopsis. The Plant Cell 19, 351–368.
| The acyltransferase GPAT5 is required for the synthesis of suberin in seed coat and root of Arabidopsis.Crossref | GoogleScholarGoogle Scholar |
Beisson F, Li-Beisson Y, Pollard M (2012) Solving the puzzles of cutin and suberin polymer biosynthesis. Current Opinion in Plant Biology 15, 329–337.
| Solving the puzzles of cutin and suberin polymer biosynthesis.Crossref | GoogleScholarGoogle Scholar |
Bernards MA (2002) Demystifying suberin. Canadian Journal of Botany 80, 227–240.
| Demystifying suberin.Crossref | GoogleScholarGoogle Scholar |
Bernards MA, Summerhurst DK, Razem FA (2004) Oxidases, peroxidases and hydrogen peroxide: the suberin connection. Phytochemistry Reviews 3, 113–126.
| Oxidases, peroxidases and hydrogen peroxide: the suberin connection.Crossref | GoogleScholarGoogle Scholar |
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.
| CYP86B1 is required for very long chain ω-hydroxyacid and α,ω-dicarboxylic acid synthesis in root and seed suberin polyester.Crossref | GoogleScholarGoogle Scholar |
Domergue F, Vishwanath SJ, Joubès J, Ono J, Lee JA, Bourdon M, Alhattab R, Lowe C, Pascal S, Lessire R, Rowland O (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.
| Three Arabidopsis fatty acyl-coenzyme A reductases, FAR1, FAR4, and FAR5, generate primary fatty alcohols associated with suberin deposition.Crossref | GoogleScholarGoogle Scholar |
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.
| 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.Crossref | GoogleScholarGoogle Scholar |
Han XY, Mao LC, Wei XP, Lu WJ (2017) Stimulatory involvement of abscisic acid in wound suberization of postharvest kiwifruit. Scientia Horticulturae 224, 244–250.
| Stimulatory involvement of abscisic acid in wound suberization of postharvest kiwifruit.Crossref | GoogleScholarGoogle Scholar |
Han XY, Lu WJ, Wei XP, Li L, Mao LC, Zhao YY (2018a) Proteomics analysis to understand the ABA stimulation of wound suberization in kiwifruit. Journal of Proteomics 173, 42–51.
| Proteomics analysis to understand the ABA stimulation of wound suberization in kiwifruit.Crossref | GoogleScholarGoogle Scholar |
Han XY, Mao LC, Lu WJ, Tao XY, Wei XP, Luo ZS (2018b) Abscisic acid induces differential expression of genes involved in wound-induced suberization in postharvest tomato fruit. Journal of Integrative Agriculture 17, 2670–2682.
| Abscisic acid induces differential expression of genes involved in wound-induced suberization in postharvest tomato fruit.Crossref | GoogleScholarGoogle Scholar |
Han XY, Mao LC, Lu WJ, Wei XP, Ying TJ, Luo ZS (2019) Positive regulation of the transcription of AchnKCS by a bZIP Transcription factor in response to ABA-stimulated suberization of Kiwifruit. Journal of Agricultural and Food Chemistry 67, 7390–7398.
| Positive regulation of the transcription of AchnKCS by a bZIP Transcription factor in response to ABA-stimulated suberization of Kiwifruit.Crossref | GoogleScholarGoogle Scholar |
Han XY, Wei XP, Lu WJ, Wu Q, Mao LC, Luo ZS (2022) Transcriptional regulation of KCS gene by bZIP29 and MYB70 transcription factors during ABA-stimulated wound suberization of kiwifruit (Actinidia deliciosa). BMC Plant Biology 22, 2–11.
| Transcriptional regulation of KCS gene by bZIP29 and MYB70 transcription factors during ABA-stimulated wound suberization of kiwifruit (Actinidia deliciosa).Crossref | GoogleScholarGoogle Scholar |
Höfer R, Briesen I, Beck M, Pinot F, Schreiber L, Franke R (2008) The Arabidopsis cytochrome P450 CYP86A1 encodes a fatty acid ω-hydroxylase involved in suberin monomer biosynthesis. Journal of Experimental Botany 59, 2347–2360.
| The Arabidopsis cytochrome P450 CYP86A1 encodes a fatty acid ω-hydroxylase involved in suberin monomer biosynthesis.Crossref | GoogleScholarGoogle Scholar |
Kumar GNM, Lulai EC, Suttle JC, Knowles NR (2010) Age-induced loss of wound-healing ability in potato tubers is partly regulated by ABA. Planta 232, 1433–1445.
| Age-induced loss of wound-healing ability in potato tubers is partly regulated by ABA.Crossref | GoogleScholarGoogle Scholar |
Landgraf R, Smolka U, Altmann S, Eschen-Lippold L, Senning M, Sonnewald S, Weigel B, Frolova N, Strehmel N, Hause G, Scheel D, Böttcher C, Rosahl S (2014) The ABC transporter ABCG1 is required for suberin formation in potato tuber periderm. The Plant Cell 26, 3403–3415.
| The ABC transporter ABCG1 is required for suberin formation in potato tuber periderm.Crossref | GoogleScholarGoogle Scholar |
Lee SB, Jung SJ, Go YS, Kim HU, Kim JK, Cho HJ, Park OK, Suh MC (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.
| 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.Crossref | GoogleScholarGoogle Scholar |
Legay S, Guerriero G, André C, Guignard C, Cocco E, Charton S, Boutry M, Rowland O, Hausman J-F (2016) MdMyb93 is a regulator of suberin deposition in russeted apple fruit skins. New Phytologist 212, 977–991.
| MdMyb93 is a regulator of suberin deposition in russeted apple fruit skins.Crossref | GoogleScholarGoogle Scholar |
Leide J, Hildebrandt U, Hartung W, Riederer M, Vogg G (2012) Abscisic acid mediates the formation of a suberized stem scar tissue in tomato fruits. New Phytologist 194, 402–415.
| Abscisic acid mediates the formation of a suberized stem scar tissue in tomato fruits.Crossref | GoogleScholarGoogle Scholar |
Li XA, Li ML, Wang L, Wang J, Jin P, Zheng YH (2018) Methyl jasmonate primes defense responses against wounding stress and enhances phenolic accumulation in fresh-cut pitaya fruit. Postharvest Biology and Technology 145, 101–107.
| Methyl jasmonate primes defense responses against wounding stress and enhances phenolic accumulation in fresh-cut pitaya fruit.Crossref | GoogleScholarGoogle Scholar |
Liu C, Peng LT, Yang SZ (2020) Effect of β-aminobutyric acid combined with sodium bicarbonate on callus of yam. Journal of Huazhong Agricultural University 39, 113–119.
Lulai EC, Corsini DL (1998) Differential deposition of suberin phenolic and aliphatic domains and their roles in resistance to infection during potato tuber (Solanum tuberosum L.) wound-healing. Physiological and Molecular Plant Pathology 53, 209–222.
| Differential deposition of suberin phenolic and aliphatic domains and their roles in resistance to infection during potato tuber (Solanum tuberosum L.) wound-healing.Crossref | GoogleScholarGoogle Scholar |
Lulai EC, Neubauer JD (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.
| Wound-induced suberization genes are differentially expressed, spatially and temporally, during closing layer and wound periderm formation.Crossref | GoogleScholarGoogle Scholar |
Lulai EC, Suttle JC, Pederson SM (2008) Regulatory involvement of abscisic acid in potato tuber wound-healing. Journal of Experimental Botany 59, 1175–1186.
| Regulatory involvement of abscisic acid in potato tuber wound-healing.Crossref | GoogleScholarGoogle Scholar |
Lulai E, Huckle L, Neubauer J, Suttle J (2011) Coordinate expression of AOS genes and JA accumulation: JA is not required for initiation of closing layer in wound healing tubers. Journal of Plant Physiology 168, 976–982.
| Coordinate expression of AOS genes and JA accumulation: JA is not required for initiation of closing layer in wound healing tubers.Crossref | GoogleScholarGoogle Scholar |
Philippe G, Sørensen I, Jiao C, Sun XP, Fei ZJ, Domozych DS, Rose JKC (2020) Cutin and suberin: assembly and origins of specialized lipidic cell wall scaffolds. Current Opinion in Plant Biology 55, 11–20.
| Cutin and suberin: assembly and origins of specialized lipidic cell wall scaffolds.Crossref | GoogleScholarGoogle Scholar |
Pollard M, Beisson F, Li YH, Ohlrogge JB (2008) Building lipid barriers: biosynthesis of cutin and suberin. Trends in Plant Science 13, 236–246.
| Building lipid barriers: biosynthesis of cutin and suberin.Crossref | GoogleScholarGoogle Scholar |
Ranathunge K, Schreiber L, Franke R (2011) Suberin research in the genomics era—new interest for an old polymer. Plant Science 180, 399–413.
| Suberin research in the genomics era—new interest for an old polymer.Crossref | GoogleScholarGoogle Scholar |
Razem FA, Bernards MA (2002) Hydrogen peroxide is required for poly(phenolic) domain formation during wound-induced suberization. Journal of Agricultural and Food Chemistry 50, 1009–1015.
| Hydrogen peroxide is required for poly(phenolic) domain formation during wound-induced suberization.Crossref | GoogleScholarGoogle Scholar |
Reid KE, Olsson N, Schlosser J, Peng F, Lund ST (2006) An optimized grapevine RNA isolation procedure and statistical determination of reference genes for real-time RT-PCR during berry development. BMC Plant Biology 6, 27
| An optimized grapevine RNA isolation procedure and statistical determination of reference genes for real-time RT-PCR during berry development.Crossref | GoogleScholarGoogle Scholar |
Rupasinghe SG, Duan H, Schuler MA (2007) Molecular definitions of fatty acid hydroxylases in Arabidopsis thaliana. Proteins 68, 279–293.
| Molecular definitions of fatty acid hydroxylases in Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar |
Serra O, Soler M, Hohn C, Sauveplane V, Pinot F, Franke R, Schreiber L, Prat S, Molinas M, Figueras M (2009) CYP86A33-targeted gene silencing in potato tuber alters suberin composition, distorts suberin lamellae, and impairs the periderm’s water barrier function. Plant Physiology 149, 1050–1060.
| CYP86A33-targeted gene silencing in potato tuber alters suberin composition, distorts suberin lamellae, and impairs the periderm’s water barrier function.Crossref | GoogleScholarGoogle Scholar |
Shukla V, Barberon M (2021) Building and breaking of a barrier: suberin plasticity and function in the endodermis. Current Opinion in Plant Biology 64, 102153
| Building and breaking of a barrier: suberin plasticity and function in the endodermis.Crossref | GoogleScholarGoogle Scholar |
Suttle JC, Lulai EC, Huckle LL, Neubauer JD (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.
| Wounding of potato tubers induces increases in ABA biosynthesis and catabolism and alters expression of ABA metabolic genes.Crossref | GoogleScholarGoogle Scholar |
Tao XY, Mao LC, Li JY, Chen JX, Lu WJ, Huang S (2016) Abscisic acid mediates wound-healing in harvested tomato fruit. Postharvest Biology and Technology 118, 128–133.
| Abscisic acid mediates wound-healing in harvested tomato fruit.Crossref | GoogleScholarGoogle Scholar |
Ursache R, De Jesus Vieira Teixeira C, Dénervaud Tendon V, Gully K, De Bellis D, Schmid-Siegert E, Grube Andersen T, Shekhar V, Calderon S, Pradervand S, Nawrath C, Geldner N, Vermeer JEM (2021) GDSL-domain proteins have key roles in suberin polymerization and degradation. Nature Plants 7, 353–364.
| GDSL-domain proteins have key roles in suberin polymerization and degradation.Crossref | GoogleScholarGoogle Scholar |
Vishwanath SJ, Kosma DK, Pulsifer IP, Scandola S, Pascal S, Joubès J, Dittrich-Domergue F, Lessire R, Rowland O, Domergue F (2013) Suberin-associated fatty alcohols in Arabidopsis: distributions in roots and contributions to seed coat barrier properties. Plant Physiology 163, 1118–1132.
| Suberin-associated fatty alcohols in Arabidopsis: distributions in roots and contributions to seed coat barrier properties.Crossref | GoogleScholarGoogle Scholar |
Vishwanath SJ, Delude C, Domergue F, Rowland O (2015) Suberin: biosynthesis, regulation, and polymer assembly of a protective extracellular barrier. Plant Cell Reports 34, 573–586.
| Suberin: biosynthesis, regulation, and polymer assembly of a protective extracellular barrier.Crossref | GoogleScholarGoogle Scholar |
Wang B, Jiang H, Bi Y, He XF, Wang Y, Li YC, Zheng XY, Prusky D (2019) Preharvest multiple sprays with sodium nitroprusside promote wound healing of harvested muskmelons by activation of phenylpropanoid metabolism. Postharvest Biology and Technology 158, 110988
| Preharvest multiple sprays with sodium nitroprusside promote wound healing of harvested muskmelons by activation of phenylpropanoid metabolism.Crossref | GoogleScholarGoogle Scholar |
Wang PT, Shan N, Ali A, Sun JY, Luo S, Xiao Y, Wang SL, Hu R, Huang YJ, Zhou QH (2022) Comprehensive evaluation of functional components, biological activities, and minerals of yam species (Dioscorea polystachya and D. alata) from China. LWT – Food Science and Technology 168, 113964
| Comprehensive evaluation of functional components, biological activities, and minerals of yam species (Dioscorea polystachya and D. alata) from China.Crossref | GoogleScholarGoogle Scholar |
Wang Z, Zhao SN, Tao SY, Hou GG, Zhao FL, Tan SP, Meng QG (2023) Dioscorea spp.: bioactive compounds and potential for the treatment of inflammatory and metabolic diseases. Molecules 28, 2878
| Dioscorea spp.: bioactive compounds and potential for the treatment of inflammatory and metabolic diseases.Crossref | GoogleScholarGoogle Scholar |
Wei XP, Mao LC, Wei XB, Xia M, Xu CJ (2020a) MYB41, MYB107, and MYC2 promote ABA-mediated primary fatty alcohol accumulation via activation of AchnFAR in wound suberization in kiwifruit. Horticulture Research 7, 86
| MYB41, MYB107, and MYC2 promote ABA-mediated primary fatty alcohol accumulation via activation of AchnFAR in wound suberization in kiwifruit.Crossref | GoogleScholarGoogle Scholar |
Wei XP, Mao LC, Lu WJ, Wei XB, Han XY, Guan WL, Yang YJ, Zha M, Xu CJ, Luo ZS (2020b) Three transcription activators of ABA signaling positively regulate suberin monomer synthesis by activating cytochrome P450 CYP86A1 in Kiwifruit. Frontiers in Plant Science 10, 1650
| Three transcription activators of ABA signaling positively regulate suberin monomer synthesis by activating cytochrome P450 CYP86A1 in Kiwifruit.Crossref | GoogleScholarGoogle Scholar |
Wei XB, Guan WL, Yang YJ, Shao YL, Mao LC (2021) Methyl jasmonate promotes wound healing by activation of phenylpropanoid metabolism in harvested kiwifruit. Postharvest Biology and Technology 175, 111472
| Methyl jasmonate promotes wound healing by activation of phenylpropanoid metabolism in harvested kiwifruit.Crossref | GoogleScholarGoogle Scholar |
Wei XB, Mao LC, Wei XP, Guan WL, Chen RC, Luo ZS (2022) AchMYC2 promotes JA-mediated suberin polyphenolic accumulation via the activation of phenylpropanoid metabolism-related genes in the wound healing of kiwifruit (Actinidia chinensis). Postharvest Biology and Technology 188, 111896
| AchMYC2 promotes JA-mediated suberin polyphenolic accumulation via the activation of phenylpropanoid metabolism-related genes in the wound healing of kiwifruit (Actinidia chinensis).Crossref | GoogleScholarGoogle Scholar |
Woolfson KN, Haggitt ML, Zhang YN, Kachura A, Bjelica A, Rey Rincon MA, Kaberi KM, Bernards MA (2018) Differential induction of polar and non-polar metabolism during wound-induced suberization in potato (Solanum tuberosum L.) tubers. The Plant Journal 93, 931–942.
| Differential induction of polar and non-polar metabolism during wound-induced suberization in potato (Solanum tuberosum L.) tubers.Crossref | GoogleScholarGoogle Scholar |
Woolfson KN, Esfandiari M, Bernards MA (2022) Suberin biosynthesis, assembly, and regulation. Plants 11, 555
| Suberin biosynthesis, assembly, and regulation.Crossref | GoogleScholarGoogle Scholar |
Xin AZ, Herburger K (2021) Mini review: transport of hydrophobic polymers into the plant apoplast. Frontiers in Plant Science 11, 590990
| Mini review: transport of hydrophobic polymers into the plant apoplast.Crossref | GoogleScholarGoogle Scholar |
Yadav V, Molina I, Ranathunge K, Castillo IQ, Rothstein SJ, Reed JW (2014) ABCG transporters are required for suberin and pollen wall extracellular barriers in Arabidopsis. The Plant Cell 26, 3569–3588.
| ABCG transporters are required for suberin and pollen wall extracellular barriers in Arabidopsis.Crossref | GoogleScholarGoogle Scholar |
Yang WL, Bernards MA (2006) Wound-induced metabolism in potato (Solanum tuberosum) tubers: biosynthesis of aliphatic domain monomers. Plant Signaling & Behavior 1, 59–66.
| Wound-induced metabolism in potato (Solanum tuberosum) tubers: biosynthesis of aliphatic domain monomers.Crossref | GoogleScholarGoogle Scholar |
Yang WL, Simpson JP, Li-Beisson Y, Beisson F, Pollard M, Ohlrogge JB (2012) A land-plant-specific glycerol-3-phosphate acyltransferase family in Arabidopsis: substrate specificity, sn-2 preference, and evolution. Plant Physiology 160, 638–652.
| A land-plant-specific glycerol-3-phosphate acyltransferase family in Arabidopsis: substrate specificity, sn-2 preference, and evolution.Crossref | GoogleScholarGoogle Scholar |
Zeng XX, Liu DH, Huang LQ (2021) Metabolome profiling of eight Chinese yam (Dioscorea polystachya Turcz.) varieties reveals metabolite diversity and variety specific uses. Life 11, 687
| Metabolome profiling of eight Chinese yam (Dioscorea polystachya Turcz.) varieties reveals metabolite diversity and variety specific uses.Crossref | GoogleScholarGoogle Scholar |
Zhou FH, Jiang AL, Feng K, Gu ST, Xu DY, Hu WZ (2019) Effect of methyl jasmonate on wound healing and resistance in fresh-cut potato cubes. Postharvest Biology and Technology 157, 110958
| Effect of methyl jasmonate on wound healing and resistance in fresh-cut potato cubes.Crossref | GoogleScholarGoogle Scholar |
