Coinfection and in vitro interaction of Lasiodiplodia pseudotheobromae and Pestalotiopsis mangiferae associated with dieback in branches of mango (Mangifera indica) Manila variety, in Veracruz, Mexico

Liliana Eunice Saucedo-Picazo, Luis Guillermo Hernández-Montiel, Norma Flores-Estévez, Patricia Gerez-Fernández, Angel Fernando Argüello-Ortiz, Juan Carlos Noa-Carrazana

Abstract


Dieback disease caused by fungal complexes is a severe problem in mango trees (Mangifera indica). Its main symptoms are branch rot, gummosis, and finally, the tree’s death. In this work, the species of the fungal complex causing mango dieback in the Manila variety in Veracruz, Mexico were identified. The in vitro interaction of two species belonging to the complex was evaluated and the severity of the co-infection in mango branches. Lasiodiplodia pseudotheobromae and Pestalotiopsis mangiferae were identified as causal agents of mango dieback in the producing area of Veracruz. In coinfected mango branches, greater severity of necrosis was observed than in individual infections. Liquid culture filtrates applied in co-cultures showed different results for each species of phytopathogen. The P. mangiferae filtrate had no significant antagonistic effects on the growth of L. pseudotheobromae (inhibition of 2.68%), while the L. pseudotheobromae filtrate inhibited 41.38% of P. mangiferae. The results show that multiple infections in mango trees increase the damage caused by dieback, which could directly impact the development of control strategies.


Keywords


gummosis; virulence; interaction; fungal complex

Full Text:

PDF

References


Abdullah AS, Moffat CS, Lopez-Ruiz FJ, Gibberd MR, Hamblin J, and Zerihun A. 2017. Host–multi-pathogen warfare: Pathogen interactions in co-infected plants. Frontiers in Plant Science 8: 1806. https://doi.org/10.3389/fpls.2017.01806

Abdullah AS, Turo C, Moffat CS, Lopez-Ruiz FJ, Gibberd MR, Hamblin J, and Zerihun A. 2018. Real-time PCR for diagnosing and quantifying co-infection by two globally distributed fungal pathogens of wheat. Frontiers in Plant Science 1086. https://doi.org/10.3389/fpls.2018.01086

Abro MA, Sun X, Li X, Jatoi GH and Guo LD. 2019. Biocontrol potential of fungal endophytes against Fusarium oxysporum f. sp. cucumerinum causing wilt in cucumber. The Plant Pathology Journal 235(6):598-608. https://doi.org/10.5423/PPJ.OA.05.2019.0129

Al-Adawi A, Deadman M, Al-Rawahi A, Al-Maqbali Y, Al-Jahwari A, Al-Saadi B, Al-Amri I, and Wingfield M. 2006. Aetiology and causal agents of mango sudden decline disease in the Sultanate of Oman. European Journal of Plant Pathology 116(4): 247-254. https://doi.org/10.1007/s10658-006-9056-x

Al-Saadoon, AH, Ameen M, Hameed M, and Al-Badran A. 2012. Histopathology of grapevine inoculated with Lasiodiplodia theobromae. Basrah Journal of Agricultural Sciences 25(1):1-12. https://doi.org/10.33762/bagrs.2012.54726

Altendorf S. 2019. Major tropical fruits market review. 2017. Rome, FAO. 10 pp. Licence: CC BY-NC-SA 3.0 IGO

Boddy, L. 2016. Chapter 10—Interactions between fungi and other microbes. En S. C. Watkinson, L. Boddy, y N. P. Money (Eds.), The Fungi (Third Edition). Academic Press. pp. 337-360. https://doi.org/10.1016/B978-0-12-382034-1.00010-4

Borrero C, Castaño R and Avilés M. 2018. First report of Pestalotiopsis clavispora (Neopestalotiopsis clavispora) causing canker and twig dieback on blueberry bushes in Spain. Plant Disease 102(6), 1178-1178. https://doi.org/10.1094/PDIS-10-17-1529-PDN

Chen F, Lu L, Ni H, Wang Y, Wang Y and Li G. 2012. First report of Pestalotiopsis mangiferae and P. vismiae causing twig dieback of Myrica rubra in China. Plant Disease 96(4): 588-588. https://doi.org/10.1094/PDIS-12-11-1054-PDN

Cimmino A, Cinelli T, Masi M, Reveglia P, da-Silva MA, Mugnai L, Michereff SJ, Surico G, and Evidente A. 2017. Phytotoxic lipophilic metabolites produced by grapevine strains of Lasiodiplodia species in Brazil. Journal of Agricultural and Food Chemistry 65(6): 1102-1107. https://doi.org/10.1021/acs.jafc.6b04906

Clendenin I. 1896. Lasiodiplodia E. and E., n. gen. Botanical Gazette 21(2): 92-92. https://doi.org/10.1086/327307

de-Oliveira CVS, Michereff SJ, Martins RB, Gava CAT, Mizubuti ESG and Câmara MPS. 2010. Species of Botryosphaeriaceae associated on mango in Brazil. European Journal of Plant Pathology 127(4): 509-519. https://doi.org/10.1007/s10658-010-9616-y

Elqassas R, and Abu-Naser SS. 2018. Expert system for the diagnosis of mango diseases. International Journal of Academic Engineering Research 2(8): 10-18

Fan S, Huang Y, Zhang X, Chen G, Zhou J, Li X, and Han M. 2019. First report of Botryosphaeria dothidea causing canker on Cotinus coggygria in China. Plant Disease 103(10): 2678-2678. https://doi.org/10.1094/PDIS-04-19-0690-PDN

Fang X, Zhang C, Wang Z, Duan T, Yu B, Jia X, Pang J, Ma L, Wang Y, and Nan Z. 2021. Co-infection by soil-borne fungal pathogens alters disease responses among diverse alfalfa varieties. Frontiers in Microbiology 12: 664385-664385. https://doi.org/10.3389/fmicb.2021.664385

Hajieghrari B, Torabi-Giglou M, Mohammadi MR, and Davari M. 2008. Biological potential of some Iranian Trichoderma isolates in the control of soil borne plant pathogenic fungi. African Journal of Biotechnology 7(8). http://www.academicjournals.org/AJB

Hoffmann A, Lischeid G, Koch M, Lentzsch P, Sommerfeld T, and Müller MEH. 2021. Co-cultivation of Fusarium, Alternaria, and Pseudomonas on wheat-Ears affects microbial frowth and mycotoxin production. Microorganisms 9(2). https://doi.org/10.3390/microorganisms9020443

Ismail AM, Cirvilleri G, Polizzi G, Crous PW, Groenewald JZ and Lombard L. 2012. Lasiodiplodia species associated with dieback disease of mango (Mangifera indica) in Egypt. Australasian Plant Pathology 41(6): 649-660. https://doi.org/10.1007/s13313-012-0163-1

Jackson DSM and Johnson-Cicalese J. 1988. A rapid staining method for detection of endophytic fungi in turf and forage grasses. Phytopathology78 237-239. https://doi.org/10.1094/Phyto-78-237

Junaid M, Purwantara A and Guest D. 2020. First report of vascular streak dieback symptom of cocoa caused by Ceratobasidium theobromae in Barru District, South Sulawesi. In IOP Conference Series: Earth and Environmental Science 486(1): 012170. https://iopscience.iop.org/article/10.1088/1755-1315/486/1/012170/pdf

Khaskheli M, Jiskani M, Soomro M, Talpur M and Poussio G. 2011. Prevalence of mango Sudden decline/death syndrome (MSDS) on various varieties at the orchards of different age in the Vicinity of Tando Qaiser, Hyderabad, Sindh. Pakistan Journal of Agriculture Agricultural Engineering and Veterinary Sciences 27(2): 160-167

Kim H, Castellon-Chicas MJ, Arbizu S, Talcott S, Drury NL, Smith S and Mertens-Talcott S. U. 2021. Mango (Mangifera indica L.) Polyphenols: Anti-Inflammatory Intestinal Microbial Health Benefits, and Associated Mechanisms of Actions. Molecules 26(9): 2732. https://doi.org/10.3390/molecules26092732

Kwon JH, Choi O, Kang B, Lee Y, Park J, Kang DW, Han I and Kim J. 2017. Identification of Lasiodiplodia pseudotheobromae causing mango dieback in Korea. Canadian Journal of Plant Pathology 39(2): 241-245. https://doi.org/10.1080/07060661.2017.1329231

Lawrence DP, Travadon R, and Baumgartner K. 2018. Novel Seimatosporium species from grapevine in northern California and their interactions with fungal pathogens involved in the trunk-disease complex. Plant Disease 102(6): 1081-1092. https://doi.org/10.1094/PDIS-08-17-1247-RE

Lee SB. 1990. Isolation of DNA from fungal mycelia and single spores. PCR protocols, a guide to methods and applications. Academic Press. 282–7. https://doi.org/10.1016/B978-0-12-372180-8.50038-X

Lerch-Olson ER and Robertson AE. 2020. Effect of co-inoculations with Pythium and Fusarium species on seedling disease development of soybean. Canadian Journal of Plant Pathology 42(3): 408-418. https://doi.org/10.1080/07060661.2019.1668858

Li L, Mohd MH, Mohamed NN, Subramaniam S and Latiffah Z. 2021. Identification of Botryosphaeriaceae associated with stem?end rot of mango (Mangifera indica) in Malaysia. Journal of Applied Microbiology 130(4): 1273-1284. https://doi.org/10.1111/jam.14828

Liu H, Macdonald CA, Cook J, Anderson IC and Singh BK. 2019. An ecological loop: host microbiomes across multitrophic interactions. Trends in Ecology and Evolution 34(12): 1118-1130. https://doi.org/10.1016/j.tree.2019.07.011

Luo F, Zhong Z, Liu L, Igarashi Y, Xie D and Li N. 2017. Metabolomic differential analysis of interspecific interactions among white rot fungi Trametes versicolor, Dichomitus squalens and Pleurotus ostreatus. Scientific Reports 7(1): 1-11. https://doi.org/10.1038/s41598-017-05669-3

Manter DK and Vivanco JM. 2007. Use of the ITS primers, ITS1F and ITS4, to characterize fungal abundance and diversity in mixed-template samples by qPCR and length heterogeneity analysis. Journal of Microbiological Methods 71(1): 7-14. https://doi.org/10.1016/j.mimet.2007.06.016

Maharachchikumbura SS, Hyde KD, Groenewald JZ, Xu J and Crous PW. 2014. Pestalotiopsis revisited. Studies in Mycology 79: 121-186. https://doi.org/10.1016/j.simyco.2014.09.005

Marques MW, Lima NB, de-Morais MA, Barbosa MAG, Souza BO, Michereff SJ, Phillips AJL and Câmara MPS. 2013. Species of Lasiodiplodia associated with mango in Brazil. Fungal Diversity 61(1): 181-193. https://doi.org/10.1007/s13225-013-0231-z

Morales-Sánchez V, Díaz CE, Trujillo E, Olmeda SA, Valcarcel F, Muñoz R and González-Coloma A. 2021. Bioactive metabolites from the endophytic fungus Aspergillus sp. SPH2. Journal of Fungi 7(2):109. https://doi.org/10.3390/jof7020109

Müller M, Steier I, Köppen R, Siegel D, ProskeM, Korn U and Koch M. 2012. Cocultivation of phytopathogenic Fusarium and Alternaria strains affects fungal growth and mycotoxin production. Journal of Applied Microbiology 113(4): 874-887. https://doi.org/10.1111/j.1365-2672.2012.05388.x

Nalin Rathnayake GR, Savitri KN, Jayasinghe L, Araya H and Fujimoto Y. 2019. Secondary metabolites produced by an endophytic fungus Pestalotiopsis microspora. Natural Products and Bioprospecting 9(6): 411-417. https://doi.org/10.1007/s13659-019-00225-0

Naglot A, Goswami S, Rahman I, Shrimali DD, Yadav KK, Gupta VK, Rabha AJ, Gogoi HK and Vee V. 2015. Antagonistic potential of native Trichoderma viride strain against potent tea fungal pathogens in North East India. The Plant Pathology Journal 31(3): 278-289. PubMed. https://doi.org/10.5423/PPJ.OA.01.2015.0004

Orton ES and Brown JKM. 2016. Reduction of growth and reproduction of the biotrophic fungus Blumeria graminis in the presence of a necrotrophic pathogen. Frontiers in Plant Science 7: 742. https://doi.org/10.3389/fpls.2016.00742

Pradeep FS, Begam MS, Palaniswamy M and Pradeep BV. 2013. Influence of culture media on growth and pigment production by Fusarium moniliforme KUMBF1201 isolated from paddy field soil. World Applied Sciences Journal 22(1):70-77. https://doi.org/10.5829/idosi.wasj.2013.22.01.7265

Qian CD, Fu YH, Jiang FS, Xu ZH, Cheng DQ, Ding B, Gao CX and Ding ZS. 2014. Lasiodiplodia sp. ME4-2, an endophytic fungus from the floral parts of Viscum coloratum, produces indole-3-carboxylic acid and other aromatic metabolites. BMC Microbiology 14: 297. https://doi.org/10.1186/s12866-014-0297-0

Qian YX, Kang JC, Luo YK, Yang XB, He J and Wang L. 2021. Secondary metabolites from endophytic Pestalotiopsis microspora and their P-Glycoprotein inhibitory activity. Chemistry of Natural Compounds 57(5): 924-926. https://doi.org/10.1007/s10600-021-03513-9

Rakesh A, Mishra JP, Prasad R, Sekhar JC, Gupta D, Reddy VP and Kumar S. 2020. Isolation and in vitro evaluation of fungicides against Pestalotiopsis mangiferae causing grey blight of mango. Journal of Pharmacognosy and Phytochemistry 9(4): 1368-1370. https://www.phytojournal.com/archives/2020/vol9issue4/PartS/9-4-145-386.pdf

Reveglia P, Masi M and Evidente A. 2020. Melleins-Intriguing natural compounds. Biomolecules 10(5): 772. https://doi.org/10.3390/biom10050772

Rodríguez-Gálvez E, Guerrero P, Barradas C, Crous PW and Alves A. 2017. Phylogeny and pathogenicity of Lasiodiplodia species associated with dieback of mango in Peru. Fungal Biology 121(4): 452-465. https://doi.org/10.1016/j.funbio.2016.06.004

Rodríguez-Gálvez E, Hilário S, Lopes A and Alves A. 2020. Diversity and pathogenicity of Lasiodiplodia and Neopestalotiopsis species associated with stem blight and dieback of blueberry plants in Peru. European Journal of Plant Pathology 157(1): 89-102. https://doi.org/10.1007/s10658-020-01983-1

Sakalidis ML, Ray JD, Lanoiselet V, Hardy GE and Burgess TI. 2011. Pathogenic Botryosphaeriaceae associated with Mangifera indica in the Kimberley region of Western Australia. European Journal of Plant Pathology 130(3): 379-391. https://doi.org/10.1007/s10658-011-9760-z

Salvatore MM, Alves A and Andolfi A. 2020. Secondary metabolites of Lasiodiplodia theobromae: Distribution, chemical diversity, bioactivity, and implications of their occurrence. Toxins 12(7): 457. https://doi.org/10.3390/toxins12070457

Sandoval-Sánchez M, Nieto-Ángel D, Sandoval-Islas JS, Téliz-Ortiz D, Orozco-Santos M and Silva-Rojas H. 2013. Hongos asociados a pudrición del pedúnculo y muerte descendente del mango (Mangifera indica). Agrociencia 47(1): 61-73. http://www.scielo.org.mx/pdf/agro/v47n1/v47n1a6.pdf

Santos J, Hilário S, Pinto G and Alves A. 2021. Diversity and pathogenicity of pestalotioid fungi associated with blueberry plants in Portugal, with description of three novel species of Neopestalotiopsis. European Journal of Plant Pathology 162(3): 39-555. https://doi.org/10.1007/s10658-021-02419-0

Secretaría de Agricultura y Desarrollo Rural (SADER). 2020. El rey de las frutas tropicales: Mango. https://www.gob.mx/agricultura/articulos/el-rey-de-las-frutas-tropicales-mango

Singh HB. 2006. Trichoderma: A boon for biopesticides industry. J Mycology Plant Patholology 36: 373-384

Susi H, Barrès B, Vale PF and Laine AL. 2015. Co-infection alters population dynamics of infectious disease. Nature Communications 6: 5975. https://doi.org/10.1038/ncomms6975

Swaroop A, Bagchi M, Moriyama H and Bagchi D. 2018. Health Benefits of mango (Mangifera indica) and mangiferin. Japan Journal of Medicine 1(2):149-154. https://japanjournalofmedicine.com/health-benefits-of-mango-mangiferaindica-l-and-mangiferin/

Tollenaere C, Susi H and Laine AL. 2016. Evolutionary and epidemiological implications of multiple infection in plants. Trends in Plant Science 21(1): 80-90. https://doi.org/10.1016/j.tplants.2015.10.014

Úrbez-Torres JR, Leavitt GM, Guerrero JC, Guevara J and Gubler WD. 2008. Identification and pathogenicity of Lasiodiplodia theobromae and Diplodia seriata, the causal agents of bot canker disease of grapevines in Mexico. Plant Disease 92(4): 519-529. https://doi.org/10.1094/PDIS-92-4-0519

Wang J, Wang G, Zhang Y, Zheng B, Zhang C and Wang L. 2014. Isolation and identification of an endophytic fungus Pezicula sp. in Forsythia viridissima and its secondary metabolites. World Journal of Microbiology and Biotechnology 30(10): 2639-2644. https://doi.org/10.1007/s11274-014-1686-0




DOI: http://dx.doi.org/10.18781/R.MEX.FIT.2203-4

Refbacks

  • There are currently no refbacks.