The role of AcPGIP in the kiwifruit (Actinidia chinensis) response to Botrytis cinerea
Zhe-Xin Li
A , Min Chen A , Yu-Xiang Miao A , Qiang Li A , Yun Ren A , Wen-Lin Zhang A , Jian-Bin Lan A and Yi-Qing Liu A *
+ Author Affiliations
- Author Affiliations
A Chongqing Key Laboratory of Economic Plant Biotechnology, Collaborative Innovation Center of Special Plant Industry in Chongqing, College of Landscape Architecture and Life Science/Institute of Special Plants, Chongqing University of Arts and Sciences, Yongchuan 402160, China.
Functional Plant Biology 48(12) 1254-1263 https://doi.org/10.1071/FP21054
Submitted: 16 February 2021 Accepted: 5 September 2021 Published: 4 October 2021
© 2021 The Author(s) (or their employer(s)). Published by CSIRO Publishing
Abstract
Kiwifruit (Actinidia chinensis) is rich in nutritional and medicinal value. However, the organism responsible for grey mould, Botrytis cinerea, causes great economic losses and food safety problems to the kiwifruit industry. Understanding the molecular mechanism underlying postharvest kiwifruit responses to B. cinerea is important for preventing grey mould decay and enhancing resistance breeding. Kiwifruit cv. ‘Hongyang’ was used as experimental material. The AcPGIP gene was cloned and virus-induced gene silencing (VIGS) was used to explore the function of the polygalacturonase inhibiting protein (PGIP) gene in kiwifruit resistance to B. cinerea. Virus-induced silencing of AcPGIP resulted in enhanced susceptibility of kiwifruit to B. cinerea. Antioxidant enzymes, secondary metabolites and endogenous hormones were analysed to investigate kiwifruit responses to B. cinerea infection. Kiwifruit effectively activated antioxidant enzymes and secondary metabolite production in response to B. cinerea, which significantly increased Indole-3-acetic acid (IAA), gibberellin 3 (GA3) and abscisic acid (ABA) content relative to those in uninfected fruit. Silencing of AcPGIP enabled kiwifruit to quickly activate hormone-signaling pathways through an alternative mechanism to trigger defence responses against B. cinerea infection. These results expand our understanding of the regulatory mechanism for disease resistance in kiwifruit; further, they provide gene-resource reserves for molecular breeding of kiwifruit for disease resistance.
Keywords: AcPGIP, antioxidant enzyme activities, Botrytis cinerea, endogenous hormones, hormone-signaling pathways, kiwifruit, plant defense response, secondary metabolites, virus-induced gene silencing.
References
Akagi A, Engelberth J, Stotz HU (2010) Interaction between polygalacturonase-inhibiting protein and jasmonic acid during defense activation in tomato against Botrytis cinerea. European Journal of Plant Pathology 128, 423–428.| Interaction between polygalacturonase-inhibiting protein and jasmonic acid during defense activation in tomato against Botrytis cinerea.Crossref | GoogleScholarGoogle Scholar |
Astaneh RK, Bolandnazar S, Zaare-Nahandi F, Oustan S (2018) Effect of selenium application on phenylalanine ammonia-lyase (PAL) activity, phenol leakage and total phenolic content in garlic (Allium sativum L.) under NaCl stress. Information Processing in Agriculture 5, 339–344.
| Effect of selenium application on phenylalanine ammonia-lyase (PAL) activity, phenol leakage and total phenolic content in garlic (Allium sativum L.) under NaCl stress.Crossref | GoogleScholarGoogle Scholar |
Bardas GA, Veloukas T, Koutita O, Karaoglanidis GS (2010) Multiple resistance of Botrytis cinerea from kiwifruit to SDHIs, QoIs and fungicides of other chemical groups. Pest Management Science 66, 967–973.
| Multiple resistance of Botrytis cinerea from kiwifruit to SDHIs, QoIs and fungicides of other chemical groups.Crossref | GoogleScholarGoogle Scholar | 20730988PubMed |
Beaudoin-Eagan LD, Thorpe TA (1985) Tyrosine and phenylalanine ammonia lyase activities during shoot initiation in tobacco callus cultures. Plant Physiology 78, 438–441.
| Tyrosine and phenylalanine ammonia lyase activities during shoot initiation in tobacco callus cultures.Crossref | GoogleScholarGoogle Scholar | 16664262PubMed |
Chance B, Maehly AC (1955) [136] Assay of catalases and peroxidases. Methods in Enzymology 2, 764–775.
| [136] Assay of catalases and peroxidases.Crossref | GoogleScholarGoogle Scholar |
Chen H, Cheng Z, Wisniewski M, Liu Y, Liu J (2015) Ecofriendly hot water treatment reduces postharvest decay and elicits defense response in kiwifruit. Environmental Science and Pollution Research 22, 15037–15045.
| Ecofriendly hot water treatment reduces postharvest decay and elicits defense response in kiwifruit.Crossref | GoogleScholarGoogle Scholar | 26002370PubMed |
De Lorenzo G, Ferrari S (2002) Polygalacturonase-inhibiting proteins in defense against phytopathogenic fungi. Current Opinion in Plant Biology 5, 295–299.
| Polygalacturonase-inhibiting proteins in defense against phytopathogenic fungi.Crossref | GoogleScholarGoogle Scholar | 12179962PubMed |
Dong T, Zheng T, Fu W, Guan L, Jia H, Fang L (2020) The effect of ethylene on the color change and resistance to Botrytis cinerea infection in ‘Kyoho’ grape fruits. Foods 9, 892
| The effect of ethylene on the color change and resistance to Botrytis cinerea infection in ‘Kyoho’ grape fruits.Crossref | GoogleScholarGoogle Scholar |
El-Esawi M, Alayafi A (2019) Overexpression of StDREB2 transcription factor enhances drought stress tolerance in cotton (Gossypium barbadense L.). Genes 10, 142
| Overexpression of StDREB2 transcription factor enhances drought stress tolerance in cotton (Gossypium barbadense L.).Crossref | GoogleScholarGoogle Scholar |
Feng C, Zhang X, Wu T, Yuan B, Ding X, Yao F, Chu Z (2016) The polygalacturonase-inhibiting protein 4 (OsPGIP4), a potential component of the qBlsr5a locus, confers resistance to bacterial leaf streak in rice. Planta 243, 1297–1308.
| The polygalacturonase-inhibiting protein 4 (OsPGIP4), a potential component of the qBlsr5a locus, confers resistance to bacterial leaf streak in rice.Crossref | GoogleScholarGoogle Scholar | 26945855PubMed |
Ferrari S, Sella L, Janni M, De-Lorenzo G, Favaron F, D’Ovidio R (2012) Transgenic expression of polygalacturonase-inhibiting proteins in Arabidopsis and wheat increases resistance to the flower pathogen Fusarium graminearum. Plant Biology 14, 31–38.
| Transgenic expression of polygalacturonase-inhibiting proteins in Arabidopsis and wheat increases resistance to the flower pathogen Fusarium graminearum.Crossref | GoogleScholarGoogle Scholar | 21974721PubMed |
Fortunati E, Giovanale G, Luzi F, Mazzaglia A, Kenny JM, Torre L, Balestra GM (2017) Effective postharvest preservation of kiwifruit and romaine lettuce with a chitosan hydrochloride coating. Coatings 7, 196
| Effective postharvest preservation of kiwifruit and romaine lettuce with a chitosan hydrochloride coating.Crossref | GoogleScholarGoogle Scholar |
Giannopolitis CN, Ries SK (1977) Superoxide dismutases: I. Occurrence in higher plants. Plant Physiology 59, 309–314.
| Superoxide dismutases: I. Occurrence in higher plants.Crossref | GoogleScholarGoogle Scholar | 16659839PubMed |
Gill SS, Tuteja N (2010) Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiology and Biochemistry 48, 909–930.
| Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants.Crossref | GoogleScholarGoogle Scholar | 20870416PubMed |
Gou J, Strauss SH, Tsai CJ, Fang K, Chen Y, Jiang X, Busov VB (2010) Gibberellins regulate lateral root formation in Populus through interactions with auxin and other hormones. The Plant Cell 22, 623–639.
| Gibberellins regulate lateral root formation in Populus through interactions with auxin and other hormones.Crossref | GoogleScholarGoogle Scholar | 20354195PubMed |
Hua C, Kai K, Bi W, Shi W, Liu Y, Zhang D (2019) Curcumin induces oxidative stress in Botrytis cinerea, resulting in a reduction in gray mold decay in kiwifruit. Journal of Agricultural and Food Chemistry 67, 7968–7976.
| Curcumin induces oxidative stress in Botrytis cinerea, resulting in a reduction in gray mold decay in kiwifruit.Crossref | GoogleScholarGoogle Scholar | 31062982PubMed |
Huang Z, Li J, Zhang J, Gao Y, Hui G (2017) Physicochemical properties enhancement of Chinese kiwi fruit (Actinidia chinensis Planch) via chitosan coating enriched with salicylic acid treatment. Journal of Food Measurement and Characterization 11, 184–191.
| Physicochemical properties enhancement of Chinese kiwi fruit (Actinidia chinensis Planch) via chitosan coating enriched with salicylic acid treatment.Crossref | GoogleScholarGoogle Scholar |
Johnson DB, Moore WE, Zank LC (1961) The spectrophotometric determination of lignin in small wood samples. Tappi Journal 44, 793–798.
Li H, Smigocki AC (2018) Sugar beet polygalacturonase-inhibiting proteins with 11 LRRs confer Rhizoctonia Fusarium and Botrytis resistance in Nicotiana plants. Physiological and Molecular Plant Pathology 102, 200–208.
| Sugar beet polygalacturonase-inhibiting proteins with 11 LRRs confer Rhizoctonia Fusarium and Botrytis resistance in Nicotiana plants.Crossref | GoogleScholarGoogle Scholar |
Li W, Wang F, Wang J, Fan F, Zhu J, Yang J, Liu F, Zhong W (2015) Overexpressing CYP71Z2 enhances resistance to bacterial blight by suppressing auxin biosynthesis in rice. PLoS One 10, e0119867
| Overexpressing CYP71Z2 enhances resistance to bacterial blight by suppressing auxin biosynthesis in rice.Crossref | GoogleScholarGoogle Scholar | 25786239PubMed |
Li G, Chi M, Chen H, Sui Y, Li Y, Liu Y, Zhang X, Sun Z, Liu G, Wang Q, Liu J (2016) Stress tolerance and biocontrol performance of the yeast antagonist, Candida diversa, change with morphology transition. Environmental Science and Pollution Research 23, 2962–2967.
| Stress tolerance and biocontrol performance of the yeast antagonist, Candida diversa, change with morphology transition.Crossref | GoogleScholarGoogle Scholar | 26637302PubMed |
Liu N, Zhang X, Sun Y, Wang P, Li X, Pei Y, Li F, Hou Y (2017) Molecular evidence for the involvement of a polygalacturonase-inhibiting protein, GhPGIP1, in enhanced resistance to Verticillium and Fusarium wilts in cotton. Scientific Reports 7, 39840
| Molecular evidence for the involvement of a polygalacturonase-inhibiting protein, GhPGIP1, in enhanced resistance to Verticillium and Fusarium wilts in cotton.Crossref | GoogleScholarGoogle Scholar | 28079053PubMed |
Liu J, Sui Y, Chen H, Liu Y, Liu Y (2018) Proteomic analysis of kiwifruit in response to the postharvest pathogen, Botrytis cinerea. Frontiers in Plant Science 9, 158
| Proteomic analysis of kiwifruit in response to the postharvest pathogen, Botrytis cinerea.Crossref | GoogleScholarGoogle Scholar | 29497428PubMed |
Luo A, Bai J, Li R, Fang Y, Li L, Wang D (2019) Effects of ozone treatment on the quality of kiwifruit during postharvest storage affected by Botrytis cinerea and Penicillium expansum. Journal of Phytopathology 167, 470–478.
| Effects of ozone treatment on the quality of kiwifruit during postharvest storage affected by Botrytis cinerea and Penicillium expansum.Crossref | GoogleScholarGoogle Scholar |
Maulik A, Ghosh H, Basu S (2009) Comparative study of protein–protein interaction observed in PolyGalacturonase-Inhibiting Proteins from Phaseolus vulgaris and Glycine max and PolyGalacturonase from Fusarium moniliforme. BMC Genomics 10, S19
| Comparative study of protein–protein interaction observed in PolyGalacturonase-Inhibiting Proteins from Phaseolus vulgaris and Glycine max and PolyGalacturonase from Fusarium moniliforme.Crossref | GoogleScholarGoogle Scholar | 19958482PubMed |
Mehli L (2017) Temporal expression of a PGIP-gene in strawberry cultivars induced by wounding or by Botrytis cinerea infection. Plant Protection Science 38, 504–506.
| Temporal expression of a PGIP-gene in strawberry cultivars induced by wounding or by Botrytis cinerea infection.Crossref | GoogleScholarGoogle Scholar |
Minas IS, Tanou G, Belghazie M, Job D, Manganarist GA, Molassiotis A, Vasilakakis M (2012) Physiological and proteomic approaches to address the active role of ozone in kiwifruit post-harvest ripening. Journal of Experimental Botany 63, 2449–2464.
| Physiological and proteomic approaches to address the active role of ozone in kiwifruit post-harvest ripening.Crossref | GoogleScholarGoogle Scholar | 22268155PubMed |
Park YS, Im MH, Gorinstein S (2015) Shelf life extension and antioxidant activity of ‘Hayward’ kiwi fruit as a result of prestorage conditioning and 1-methylcyclopropene treatment. Journal of Food Science and Technology 52, 2711–2720.
| Shelf life extension and antioxidant activity of ‘Hayward’ kiwi fruit as a result of prestorage conditioning and 1-methylcyclopropene treatment.Crossref | GoogleScholarGoogle Scholar | 25892768PubMed |
Saavedra GM, Sanfuentes E, Figueroa PM, Figueroa CR (2017) Independent preharvest applications of methyl jasmonate and chitosan elicit differential upregulation of defense-related genes with reduced incidence of gray mold decay during postharvest storage of Fragaria chiloensis fruit. International Journal of Molecular Sciences 18, 1420
| Independent preharvest applications of methyl jasmonate and chitosan elicit differential upregulation of defense-related genes with reduced incidence of gray mold decay during postharvest storage of Fragaria chiloensis fruit.Crossref | GoogleScholarGoogle Scholar |
Saigne-Soulard C, Abdelli-Belhadj A, Télef-Micouleau M, Bouscaut J, Cluzet S, Corio-Costet M-F, Jean-Michel M (2015) Oligosaccharides from Botrytis cinerea and elicitation of grapevine defense. Polysaccharides 939–958.
| Oligosaccharides from Botrytis cinerea and elicitation of grapevine defense.Crossref | GoogleScholarGoogle Scholar |
Sun J, Tang W, Liu Y (2014) Transient expression of CHS-RNAi effectively influences the accumulation of anthocyanin in fruit of kiwifruit (Actinidia chinensis. Chinese Journal of Applied & Environmental Biology 20, 929–933.
| Transient expression of CHS-RNAi effectively influences the accumulation of anthocyanin in fruit of kiwifruit (Actinidia chinensis.Crossref | GoogleScholarGoogle Scholar |
Szankowski I, Briviba K, Fleschhut J, Schönherr J, Jacobsen HJ, Kiesecker H (2003) Transformation of apple (Malus domestica Borkh.) with the stilbene synthase gene from grapevine (Vitis vinifera L.) and a PGIP gene from kiwi (Actinidia deliciosa. Plant Cell Reports 22, 141–149.
| Transformation of apple (Malus domestica Borkh.) with the stilbene synthase gene from grapevine (Vitis vinifera L.) and a PGIP gene from kiwi (Actinidia deliciosa.Crossref | GoogleScholarGoogle Scholar | 14504909PubMed |
Tang J, Liu Y, Li H, Wang L, Huang K, Chen Z (2015) Combining an antagonistic yeast with harpin treatment to control postharvest decay of kiwifruit. Biological Control 89, 61–67.
| Combining an antagonistic yeast with harpin treatment to control postharvest decay of kiwifruit.Crossref | GoogleScholarGoogle Scholar |
Velikova V, Yordanov I, Edreva A (2000) Oxidative stress and some antioxidant systems in acid rain-treated bean plants: Protective role of exogenous polyamines. Plant Science 151, 59–66.
| Oxidative stress and some antioxidant systems in acid rain-treated bean plants: Protective role of exogenous polyamines.Crossref | GoogleScholarGoogle Scholar |
Wang R, Lu L, Pan X, Hu Z, Ling F, Yan Y, Liu Y, Lin Y (2015) Functional analysis of OsPGIP1 in rice sheath blight resistance. Plant Molecular Biology 87, 181–191.
| Functional analysis of OsPGIP1 in rice sheath blight resistance.Crossref | GoogleScholarGoogle Scholar | 25488398PubMed |
Xue Z, Feng W, Cao J, Cao D, Jiang W (2009) Antioxidant activity and total phenolic contents in peel and pulp of Chinese jujube (Ziziphus jujuba Mill) fruits. Journal of Food Biochemistry 33, 613–629.
| Antioxidant activity and total phenolic contents in peel and pulp of Chinese jujube (Ziziphus jujuba Mill) fruits.Crossref | GoogleScholarGoogle Scholar |
Zhang C, Feng C, Wang J, Kong F, Sun W, Wang F (2016) Cloning, expression analysis and recombinant expression of a gene encoding a polygalacturonase-inhibiting protein from tobacco, Nicotiana tabacum. Heliyon 2, e00110
| Cloning, expression analysis and recombinant expression of a gene encoding a polygalacturonase-inhibiting protein from tobacco, Nicotiana tabacum.Crossref | GoogleScholarGoogle Scholar | 27441281PubMed |
