Review: Fruit collapse and heart rot disease in pineapple: Pathogen characterization, ultrastructure infections of plant and cell mechanism resistance
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Abstract. Cano-Reinoso DM, Soesanto L, Kharisun, Wibowo C. 2021. Review: Fruit collapse and heart rot disease: Pathogen characterization, ultrastructure infections of plant and cell mechanism resistance. Biodiversitas 22: 2477-2488. Fruit collapse and bacterial heart rot are diseases in pineapple caused by Erwinia chrysanthemi (later classified as Dickeya zeae) which are increasingly prevalent in the last decade, causing devastating production loss in pineapple cultivation. Yet, comprehensive knowledge to tackle such diseases is limited, understandably due to the relatively new emerge of the diseases. Here, we review the causes of bacterial heart rot and fruit collapse, stages of infection, typical symptoms and the occurrence of resistance mechanisms in plants. In pineapple, the fruit collapse is noticeable by the release of juice and gas bubbles, also the shell of the fruit that turns into olive-green. Meanwhile, bacterial heart rot is characterized by water-soaked zones on the leaves, the formation of brown streaks on the lamina and in the mesophyll, and light-brown exudate in the blisters. The most common means of penetration into the host plant used by this type of pathogen is through plant natural openings, injuries and wounds, and entire surfaces. Concurrently, plants and fruits develop disease-resistant mechanisms to inhibit infection growth under this pathogenic attack. These mechanisms can be divided into hypersensitive reactions, locally acquired resistance, and systematic acquired resistance. In addition, pathological infections produce an interaction of the cell wall with pectolytic enzymes. Understanding the membrane breakdown process carried out by these enzymes has become critical to a pineapple protection plan. This review suggests that future research to tackle fruit collapse and bacterial heart rot can be focused on disease-resistant mechanisms, and their effects on the cell wall status with an enzymatic characterization.
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References
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Brady CL, Cleenwerck I, Denman S, Venter SN, Rodríguez-Palenzuela P, Coutinho TA, DeVos P. 2012. Proposal to reclassify Brenneria quercina (Hildebrand and Schroth 1967) Hauben et al. 1999 into a new genus, Lonsdalea gen. nov., as Lonsdalea quercina comb. nov., descriptions of Lonsdalea quercina subsp. quercina comb. nov., Lonsdalea quercina subsp. iberica subsp. nov., and Lonsdalea quercina subsp. britannica subsp. nov., emendation of the description of the genus Brenneria, reclassification of Dickeya dieffenbachiae as Dickeya dadantii subsp. dieffenbachiae comb. nov., and emendation of the description of Dickeya dadantii. Int. J. Syst. Evol. Micro. 62:1592-1602.
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Carpita NC, Gibeaut DM. 1993. Structural models of primary cell walls in flowering plants: consistency of molecular structure with the physical properties of the walls during growth. The Plant J. 3(1): 1-30.
Chen NJ, Paull RE, Chen CC. Saradhuldhat, P. 2009. Pineapple production for quality and postharvest handling. Acta Hort. 822: 253-260.
Chet I, Zilberstein Y, Henis Y. 1973. Chemotaxis of Pseudomonas lachrymans to plant extracts and to water droplets collected from the leaf surfaces of resistant and susceptible plants. Physiol. Plant Path. 3(4): 473-479.
Chinnasri B, Sipes B. 2005. Effect of a systemic acquired resistance inducer on nematodes infecting pineapple. In IV International Pineapple Symposium. University of Hawaii, 2002.
Chinnasri B, Sipes BS, Schmitt DP. 2006. Effects of inducers of systemic acquired resistance on reproduction of Meloidogyne javanica and Rotylenchulus reniformis in pineapple. J. Nemat. 38(3): 319-325.
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Huang JS. 1986. Ultrastructure of bacterial penetration in plants. Annu. Rev. Phyt. 24(1): 141-157.
Kaneshiro WS, Burger M, Vine BG, de Silva AS, Alvarez AM. 2008. Characterization of Erwinia chrysanthemi from a bacterial heart rot of pineapple outbreak in Hawaii. Plant Dis. 92(10): 1444-1450.
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Brady CL, Cleenwerck I, Denman S, Venter SN, Rodríguez-Palenzuela P, Coutinho TA, DeVos P. 2012. Proposal to reclassify Brenneria quercina (Hildebrand and Schroth 1967) Hauben et al. 1999 into a new genus, Lonsdalea gen. nov., as Lonsdalea quercina comb. nov., descriptions of Lonsdalea quercina subsp. quercina comb. nov., Lonsdalea quercina subsp. iberica subsp. nov., and Lonsdalea quercina subsp. britannica subsp. nov., emendation of the description of the genus Brenneria, reclassification of Dickeya dieffenbachiae as Dickeya dadantii subsp. dieffenbachiae comb. nov., and emendation of the description of Dickeya dadantii. Int. J. Syst. Evol. Micro. 62:1592-1602.
Burkholder WR, McFadden LA, Dimock EW. 1953. A bacterial blight of Chrysanthemums. Phytop. 43(9): 522-526.
Carpita NC, Gibeaut DM. 1993. Structural models of primary cell walls in flowering plants: consistency of molecular structure with the physical properties of the walls during growth. The Plant J. 3(1): 1-30.
Chen NJ, Paull RE, Chen CC. Saradhuldhat, P. 2009. Pineapple production for quality and postharvest handling. Acta Hort. 822: 253-260.
Chet I, Zilberstein Y, Henis Y. 1973. Chemotaxis of Pseudomonas lachrymans to plant extracts and to water droplets collected from the leaf surfaces of resistant and susceptible plants. Physiol. Plant Path. 3(4): 473-479.
Chinnasri B, Sipes B. 2005. Effect of a systemic acquired resistance inducer on nematodes infecting pineapple. In IV International Pineapple Symposium. University of Hawaii, 2002.
Chinnasri B, Sipes BS, Schmitt DP. 2006. Effects of inducers of systemic acquired resistance on reproduction of Meloidogyne javanica and Rotylenchulus reniformis in pineapple. J. Nemat. 38(3): 319-325.
Chinchilla CM, González L, Morales F. 1979. Pudrición bacteriana del cogollo de la piña en Costa Rica. Agron. Costarric 3: 183-185.
Collmer A, Berman P, Mount MS. 1982. Pectate lyase regulation and bacterial soft-rot pathogenesis. Phytop. Prokar. 1: 395-422.
Collmer A, Keen NT. 1986. The role of pectic enzymes in plant pathogenesis. Annu. Rev. Phytop. 24(1): 383-409.
Curtis LC. 1943. Deleterious effects of guttated fluids on foliage. Amer. J. Bot. 1: 778-782.
De Freitas ST, De Cássia RMRN. 2017. Calcium Treatments. In: Pareek S (eds) Novel Postharvest Treatments of Fresh. CRC Press, New York.
De Lorenzo G, Cervone F, Hahn MG, Darvill A, Albersheim P. 1991. Bacterial endopectate lyase: evidence that plant cell wall pH prevents tissue maceration and increases the half-life of elicitor-active oligogalacturonides. Phys. Mol. Plant Path. 39(5): 335-344.
Demarty M., Morvan C, Thellier M. 1984. Calcium and the cell wall. Plant, Cell Env. 7:441–448.
Esau K. 1965. Plant anatomy. Plant Anatomy. John Wiley & Sons, New York.
Everett KR, Hallett IC, Rees-George J, Chynoweth RW, Pak HA. 2008. Avocado lenticel damage: The cause and the effect on fruit quality. Posth. Bio. Tech. 48(3): 383-390.
Fox RTV, Manners JG, Myers A. 1972. Ultrastructure of tissue disintegration and host reactions in potato tubers infected by Erwinia carotovora var. atroseptica. Pot. Res. 15(2): 130-145.
Gänzle MG. 2015. Lactic metabolism revisited: metabolism of lactic acid bacteria in food fermentations and food spoilage. Curr. Opin. Food Sci. 2: 106-117.
Goñi MG, Quirós-Sauceda AE, Velderrain-Rodríguez GR, Ovando-Martínez M, Roura SI, González-Aguilar GA, Sunil Pareek. 2017. Salicylic Acid Treatments. In: Sunil Pareek (eds) Novel Postharvest Treatments of Fresh Produce. CRC Press, New York.
Grenier AM, Duport G, Pagès S, Condemine G, Rahbé Y. 2006. The phytopathogen Dickeya dadantii (Erwinia chrysanthemi 3937) is a pathogen of the pea aphid. App. Env. Micro. 72(3): 1956-1965.
Guan Y, Chang R, Liu G, Wang Y, Wu T, Han Z, Zhang X. 2015. Role of lenticels and microcracks on susceptibility of apple fruit to Botryosphaeria dothidea. Eur. J. Plant Path. 143(2): 317-330.
Gudesblat GE, Torres PS, Vojnov AA. 2009. Stomata and pathogens: Warfare at the gates. Plant Sign. Beh. 4: 1114–1116.
Hayat Q, Hayat S, Irfan M, Ahmad A. 2010. Effect of exogenous salicylic acid under changing environment: A review. Env. Exp. Bot. 68: 14–25.
Hayward P. 1974. Waxy structures in the lenticels of potato tubers and their possible effects on gas exchange. Planta 1: 273-277.
Huang JS. 1986. Ultrastructure of bacterial penetration in plants. Annu. Rev. Phyt. 24(1): 141-157.
Kaneshiro WS, Burger M, Vine BG, de Silva AS, Alvarez AM. 2008. Characterization of Erwinia chrysanthemi from a bacterial heart rot of pineapple outbreak in Hawaii. Plant Dis. 92(10): 1444-1450.
Kerns KR, Collins JL, Kim H. 1936. Developmental Studies of the Pineapple Ananas comosus (L) Merr. I. Origin and Growth of Leaves and Inflorescence. The New Phyt. 35(4): 305-317.
Kivilaan A, Bandurski RS, Schulze A. 1971. A partial characterization of an autolytically solubilized cell wall glucan. Plant Phys. 48(4): 389-393.
Kleemann L. 2016. Organic Pineapple Farming in Ghana-A Good Choice for Smallholders? The J. Dev. Areas 50(3): 109-130.
Knauss JF, Wehlburg C. The distribution and pathogenicity of Erwinia chrysanthemi Burkholder et al. to Syngonium podophyllum Schott. Proceedings of the Florida State Horticultural Society. 1969
König H, Fröhlich J. 2017. Lactic acid bacteria. In: König H, Unden G, Fröhlich J (eds) Biology of Microorganisms on Grapes, in Must and in Wine. Springer, Cham, Berlin.
Kotoujansky A. 1987. Molecular genetics of pathogenesis by soft rot Erwinias. Annu. Rev. Phyt. 25: 405-430.
Korres AMN, Ventura JA, Fernandes PMB. 2010. First report of bacterium and yeasts associated with pineapple fruit collapse in Espírito Santo State, Brazil. Plant Dis. 94(12): 1509-1509.
Lim WH. 1974. Etiology of fruit collapse and bacterial heart rot of pineapple. MARDI Res Bull Malays Agric Res Dev Inst., 2(2): 11-16.
Lim WH, Lowings PH. Infections sites of pineapple fruit collapse and latency of the pathogen, Erwinia chrysanthemi, within the fruit. In Proceedings of the 4th International Conference on Plant Pathogenic Bacteria. Angers, France, August 1978.
Lim WH, Lowings PH. 1979. Pineapple fruit collapse in Peninsular Malaysia: symptoms and varietal susceptibility. Plant Dis. Rep. 63: 170-174.
Lim WH. 1985. Diseases and disorders of pineapples in peninsular Malaysia. Malaysian Agricultural Research and Development Institute (MARDI). Report number: 97.
Marín-Rodríguez MC, Orchard J, Seymour GB. 2002. Pectate lyases, cell wall degradation and fruit softening. J. Exp. Bot. 53(377): 2115-2119.
Melo SAPD, Araujo E, Suassuna J. 1974. Preliminary note on the occurrence of Erwinia sp. causing a dry rot of pineapple fruits in Paraiba. Rev. Agr. 49: 124.
Melotto M, Underwood W, Sheng YH. 2008. Role of stomata in plant innate immunity and foliar bacterial diseases. Annu. Rev. Phyt. 46: 101–122.
Mendgen K, Hahn M, Deising H. 1996. Morphogenesis and mechanisms of penetration by plant pathogenic fungi. Annu. Rev. Phyt. 34: 367–386.
Miller HN, McFadden LA. 1961. A bacterial disease of philodendron. Phyt. 51(12): 827-831.
Meeteren VU, Aliniaeifard S. 2016. Stomata and Postharvest Physiology. In: Pareek S (eds) Postharvest Ripening Physiology of Crops. CRC Press, New York.
Mintz-Oron S, Mandel T, Rogachev I, Feldberg L, Lotan O, Yativ M, Wang Z, Jetter R, Venger I, Adato A. 2008. Gene expression and metabolism in tomato fruit surface tissues. Plant Phys. 147: 823–851.
Montanaro G, Dichio B,cXiloyannis C. 2012. Fruit transpiration: mechanisms and significance for fruit nutrition and growth. In: Montonaro G (eds) Advances in selected plant physiology aspects. IntechOpen, Rijeka.
Mount MS. 1 978. Tissue is disintegrated. Plant Dis. Adv. Treat. 3: 279-297.
Nakajima N, Ishihara K, Tanabe M, Matsubara K, Matsuura Y. 1999. Degradation of pectic substances by two pectate lyases from a human intestinal bacterium, Clostridium butyricum-beijerinckii group. J. Bios. Bioeng. 88(3): 331-333.
Paull RE, Chen CC. 2003. Postharvest Physiology, Handling and Storage of Pineapple. In: Bartholomew DP, Paull RE (eds) The Pineapple: botany, production and uses. CABI, Honolulu.
Peckham GD, Kaneshiro WS, Luu V, Berestecky JM, Alvarez AM. 2010. Specificity of monoclonal antibodies to strains of Dickeya sp. that cause bacterial heart rot of pineapple. Hybr. 29(5): 383-389.
Pierce S, Maxwell K, Griffiths H, Winter K. 2001. Hydrophobic trichome layers and epicuticular wax powders in Bromeliaceae. Amer. J. Bot. 88(8): 1371-1389.
Prasetyo J, Aeny TN. 2014. Pineapple Fruit Collapse: Newly Emerging Disease of Pineapple Fruit in Lampung, Indonesia. J. Hama Peny. Tumb. Trop. 14(1): 96-99.
Ratti MF, Ascunce MS, Landivar JJ, Goss EM. 2018. Pineapple heart rot isolates from Ecuador reveal a new genotype of Phytophthora nicotianae. Plant Path. 67(8): 1803-1813.
Raskin I. 1992. Role of salicylic acid in plants. Annu. Rev. Plant Biol. 43: 439-463.
Riederer M, Muller C. 2008. Annual Plant Reviews, Biology of the Plant Cuticle. John Wiley and Sons, New York.
Rohrbach, KG. 1984. Pineapple diseases and pests and their potential for spread. In: Singh, K.G. (Ed.), Exotic Plant Quarantine Pests and Procedures for Introduction of Plant Materials. ASEAN Plant Quarantine Centre and Training Institute. pp. 145-171.
Rohrbach KG, Johnson, MW. 2003. Pests, diseases and weeds. In: Bartholomew DP, Paull RE (eds) The Pineapple: botany, production and uses. CABI, Honolulu.
Rombouts FM, Pilnik W, Joslyn MA. 1972. Research on pectin depolymerases in the sixties?a literature review. Crit. Rev. Food Sci. Nutr. 3(1): 1-26.
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