Molecular communication in the pathosystem Capsicum species -Phytophthora capsici

Ismael Fernando Chávez-Díaz, Emma Zavaleta-Mejía

Abstract


Phytophthora capsici is a phytopathogen that limits the production of vegetables worldwide. It is known to be the causal agent of the wilting of chili pepper, which affects the plantations of the genus Capsicum, causing almost complete losses. The pathosystem Capsicum spp. – P. capsici has been widely studied, but it is still far from being understood. Investigations on different chili pepper cultivars resistant to the oomycete suggest that most genotypes carry defense genes to confront the pathogen; however, the defensive capacity differs in intensity and speed. The specific resistance of some Capsicum species to P. capsici seems to be unrelated to R proteins, but rather mediated by a complex molecular dialogue. In some species of Capsicum, the growth regulators play an important part in this dialogue that leads the plant to express the genes related to defense, locally at first, by limiting the progress of the oomycete, and later, systemically, by preventing new points of infection. This revision carries out a critical analysis of the information available on the communication network established between chili plants and P. capsici, which defines the outcome of the interaction between the plant and P. capsici as resistant, tolerant or susceptible.

Keywords


Molecular dialogue; plant immunity; plant-pathogen interaction; defense genes; growth regulators with the function of messenger molecules

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References


Bae H, Roberts DP, Lim HS, Strem MD, Park SC, Ryu CM, Meinick RL, Bailey BA. (2011). Endophytic Trichoderma isolates from tropical environments delay disease onset and induce resistance against P. capsici in hot pepper using multiple mechanisms. Mol. Plant-Microbe Interac. 24:336-351. Doi: https://doi.org/10.1094/MPMI-09-10-0221

Barchenger DW, Lamour KH, Bosland PW. (2018). Challenges and Strategies for Breeding Resistance in Capsicum annuum to the Multifarious Pathogen, Phytophthora capsici. Front. Plant Sci. 9:628. Doi: http://journal.frontiersin.org/article/10.3389/fpls.2018.00628/full

Bent AF, Makey D. (2007). Elicitors, Effectors and R genes: The new paradigm and lifetime supply of questions. Annu. Rev. Phytopathol. 45:399-436. Doi: https://doi.org/10.1146/annurev.phyto.45.062806.094427

Bertoni G. (2012). Oxylipins and plant palatability. Plant Cell. 24: 1305. Doi: https://doi.org/10.1105/tpc.112.240412

Bishop HSL, Mounter SA, Laskey J, Morris RO, Elder J, Roop P, Rouse C, Schmidt FJ, English JT. (2002). Phage-Displayed peptides as developmental agonists for Phytophthora capsici zoospores. App.Envir. Microbiol. 68:3315-3320. Doi: https://doi.org/10.1128/AEM.68.7.3315-3320.2002

Bostock RM, Saychenko C, Lazarus C, Dehesh K. (2011). Eicosapolyenoic acids. Novel MAMPs with reciprocal effect on oomycete-plant defense signaling networks. Plant Signal. Behav. 6:531-533. Doi: https://doi.org/10.4161/psb.6.4.14782

Brich PRJ, Boevink PC, Gilroy EM, Hein I, Pritchard L, Whisson SC. (2008). Oomycete RXLR effectors: delivery, functional redundancy and durable disease resistance. Curr. Opin. Plant Biol. 11:337-379. Doi: https://doi.org/10.1016/j.pbi.2008.04.005

Cannon SB, Zhu H, Baumgarte AM, Spangler R, May G, Cook DR, Young ND. (2002). Diversity, distribution and ancient taxonomic relationship within the TIR and Non-TIR NBS-LRR resistance gene subfamilies. J. Mol. Evol. 54:548-562. Doi: https://doi.org/10.1007/s0023901-0057-2

Castro-Rocha A, Fernández-Pavia SP, Osuna-Avila P. (2012) Chili defense mechanisms in the Capsicum annuum-Phytophthora capsici pathosystem. R.M.F. 30:49-65. En línea: www.scielo.org.mx/scielo.php?script=sci_arttext&pid=S0185-33092012000100005

Chemeltorit PP, Mutaqin KH, Widodo W. (2017). Combining Trichoderma hamatum THSW13 and Pseudomonas aeruginosa BJ10-86:a synergistic chili pepper seed treatment for Phytophthora capsici infested soil. Eur. J. Plant. Pathol. 147:157-166. Doi: https://doi.org/10.1007/s10658-016-0988-5

Chen YY, Chen PC, Tsay TT. (2016). The biocontrol efficacy and antibiotic activity of Streptomyces plicatus on the oomycete Phytophthora capsici. Bio. Con. 98:34-42. Doi: https://doi.org/10.1016/j.biocontrol.2016.02.011

Conrath U. (2009). Priming of induced plant defense responses. Adv. Bot. Res. 51:361-395. Doi: https://doi.org/10.1016/S0065-2296(09)51009-9

Dahiya N, Tewari R, Hoondal GS. (2006). Biotechnological aspects of chitinolytic enzymes: a review. Appl. Microbiol. Biotechnol. 71:773-782. Doi: https://doi.org/10.1007/s00253-005-0183-7

Egea C, Alcázar MD, Candela E. (1996). Capsidiol: Its role in the resistance of Capsicum annuum to P. capsici. Physiol. Plantarum. 98:737:742. Doi: https://doi.org/10.1111/j.1399-3054.1996.tb06679.x

Feng B, Li P, Wang H, Zhang X. (2010). Functional analysis of Pcpme6 fom oomycete plant pathogen Phytophthora capsici. Microb. Pathog. 49:23-31. Doi: https://doi.org/10.1016/j.micpath.2010.03.004

Fernández-Herrera E, Rojas-Martínez RI, Gómez-Rodríguez O, Guevara-Olvera L, Rivas-Dávila ME, Valdez-Moctesuma E, Zavaleta-Mejía E. (2012). Genes de defensa, actividad enzimática y contenido de capsidiol en chile CM-334 inoculado con Phytophthora capsici. Interciencia. 37:370-377. En línea: http://www.redalyc.org/articulo.oa?id=33922756007

French MRD, Jones JB, Ozores HM, Roberts PD. (2007). Survival of inoculum of Phytophthora capsici in soil trough time under different soil treatment. Plant Dis. 91:593-598. Doi: https://doi.org/10.1094/PDIS-91-5-0593

Glowacki S, Macoiszek VK, Kononowicz AK. (2011). R proteins as fundamentals of plant innate immunity. Cell. Mol. Biol. Letters. 16:1-24. Doi: https://doi.org/10.2478/s11658-010-0024-2

Goldberg NP. (2001) Chile Pepper Diseases Circular 549. College of Agriculture, Consumer and Environmental Science. New Mexico State Universiy. En línea: https://aces.nmsu.edu/pubs/_circulars/CR549/welcome.html

Gururani MA, Vankatesh J, Upadhyaya CP, Nookaraju A, Padney SK, Park SW. (2012). Plant disease resistance genes: Current status and future directions. Physiol. Mol. Plant Pathol. 78:51-65. Doi: https://doi.org/10.1016/j.pmpp.2012.01.002

Hardham AR, Shan W. (2009). Cellular and molecular biology of Phytophthora-Plant Interactions. In: Deising H (Ed.) Plant Relationships, 2nd Edition The Mycota V. Edition. Springer-Verlag Berlin. pp. 3-27. Doi: https://doi.org/10.1007/978-3-540-87407-2_1

Jiménez-Camargo A, Valadez-Moctezuma E, Lozoya-Saldaña H. (2018). Antagonism by Penicillum sp. Against Phytophthora capsici (Leonian). Rev. Fitotec. Mex. 41:137-148. En línea: https://www.revistafitotecniamexicana.org/documentos/41-2/5a.pdf

Jingyuan Z, Xuexiao Z, Zhenchuan M, Bingyan X. (2011). A novel pepper (Capsicum annuum L.) WRKY Gene CaWRKY30, is involved in pathogen stress responses. J. Plant Biol. 54:329-337. Doi: https://doi.org/10.1007/s12374-011-9171-x

Jung WJ, Jin YL, Kim KY, Park RD, Kim TH. (2005). Changes in pathogenesis-related proteins in pepper plants with regard to biological control of phytopthora blight with Paenibacillus illinoisensis. BioControl. 50:165-178. Doi: https://doi.org/10.1007/s10526-004-0451-y

Jupe J, Stam R, Howden AJM, Morrin JA, Zhang R, Hedley PE, Huitema E. (2013). Phytophthora capsici-tomato interaction features dramatic shifts gene expression associated with a hemi-biotrophic lifestyle. Genome Biol. 14:R63. Doi: https://doi.org/10.1186/gb-2013-14-6-r63

Kamoun S. (2006). A catalogue of the effector secretome of plant pathogenic oomycetes. Annu. Rev. Physiol. 44:41-60. Doi: https://doi.org/10.1146/annurev.phyto.44.070505.143436

Kim BS, Lee JY, Hwang BK. (2000). In vivo control and in vitro antifungal activiry of rhamnolipid B, a glycolipid antibiotic, against Phytophthora capsici and Colletotrichum orbiculare. 56:1029-1035. Doi: https://doi.org/10.1002/1526-4998(200012)56:12<1029::AID-PS238>3.0.CO;2-Q

Lamour KH, Stam R, Jupe J, Huitema E. (2012). The oomycete broad-host-range pathogen Phytophthora capsici. Mol. Plant Pathol. 13:329-337. Doi: https://doi.org/10.1111/j.1364-3703.2011.00754.x

Lee JH, Hong JP, Oh SK, Lee S, Choi D, Kim WT. (2004). The ethylene-responsive factor like protein 1 (CaERFLP1) of hot pepper (Capsicum annuum L.) interacts in vitro with both GCC and DRE/CRT sequence with different binding affinities possible biological roles of CaERFPL1 in response to pathogen interactions and high salinity conditions in transgenic tobacco plants. Plant. Mol. Biol. 42:335-344. Doi: https://doi.org/10.1007/s11103-004-0417-6

Lee SC, Hwang BK. (2005). Induction of some defense-related genes and oxidative burst is required for the establishment of systemic acquired resistance in Capsicum annuum. Planta. 221: 790-800. Doi: https://doi.org/10.1007/s00425-005-1488-6

Ley-López N, Márquez-Zequera I, Carrillo-Fasio JA, León-Félix J, Cruz-Lachica I, García-Estrada RS. (2018). Effect of biocontrol and germinative inhibition of Bacillus spp. On zoospores of Phytophthora capsici. RMF. 36:215-232. Doi: http://dx.doi.org/10.18781/R.MEX.FIT.1711-2

López-Martínez NM, Colinas-León T, Peña-Valdivia CB, Salinas-Moreno Y, Fuentes-Montiel P, Biesaga M, Zavaleta-Mejía E. (2011). Alterations in peroxidase activity and phenylpropanoid metabolism induced by Nacobbus aberrans Thorne and Allen in chilli (Capsicum annuum L.) CM334 resistant to Phytophthora capsici Leo. Plant and soil. 338:399-409. Doi: https://doi.org/10.1007/s11104-010-0553-5

Minamiyama Y, Tsuro M, Kubo T, Hirai M. (2005). QTL analysis for recistance to Phytophtthora capsici in pepper using a high density SSR-based map. Breed. Sci. 57:129-134. Doi: https://doi.org/10.1270/jsbbs.57.129

Mongkolporn O, Taylor PWJ. (2011). Capsicum. In: Wild Crop Relatives: Genomics and Breeding Resourses, Vegetables. (Ed) Kole, C. Springer-Verlag Berlin Heidelberg. Pp. 43-57. Doi: https://doi.org/10.1007/978-3-642-20450-0

Muthamilarasan M, Prasad M. (2013). Plant innate immunity: An updated insight into defense mechanism. J. Biosci. 38:1-17. Doi: https://doi.org/10.1007/s12038-013-9302-2

Nespoulous C, Gaudemer O, Huet JC, Pernollet JC. (1999). Characterization of elicitin-like phospholipases isolated from Phytophthora caspici culture filtrate. FEBS letters. 452:400-406. Doi: https://doi.org/10.1016/S0014-5793(99)00654-7

Ozgonen H, Yardimci N, Kilic HC. (2009). Induction of phenolic compounds and pathogenesis-related proteins by mycorrhizal fungal inoculations against Phytophthora capsici Leonian in pepper. Pak. J. Biol. Sci. 12:1181-1187. Doi: 10.3923/pjbs.2009.1181.1187. En línea: https://scialert.net/abstract/?doi=pjbs.2009.1181.1187

Ramos SRU, Gutiérrez SJG, Rodrígez GR, Salcedo MSM, Hernández LCE, Luna OHA, Jiménez BJF, Fraire VS, Almeyda LIH. (2010) Antagonismo de dos ascomicetos contra Phytophthora capsici Leonian, causante de la marchitez del chile (Capsicum annuum L.) RMF. 28:75-86. En línea: www.scielo.org.mx/scielo .php?script=sci_arttext&pid=S0185-33092010000200001

Reifschneider FJB, Boiteux LS, Della Vecchia PT. (1992). Inheritance of resisance in peppers to Phytophthora capsici in pepper. Euphytica 62:45-49. https://doi.org/10.1007/BF00036086

Sanzón-Gómez D, Zavaleta-Mejía E. (2011). Respuesta de hipersensibilidad, una muerte programada para defenderse del ataque por fitopatógeno. RMF. 29:154-164. En línea: www.scielo.org.mx/scielo.php?script=sci_arttext&pid=S018533092011000200007&lng=es&nrm=iso

Stam R, Jupe J, Howden AJM, Morris JA, Bovenik PC, Heldey PE, Huitema E. (2013). Identification and characterization CRN effectors in Phytophthora capsici show modularity and functional diversity. PLoS ONE 8(3):e59517. En línea: www.plosone.org/article/citationList.action?articleURI=info%3Adoi%2F10.1371%2Fjournal.pone.0059517

Sudisha J, Sarathchandra RG, Amrutesh KN, Kumar A, Shetty HS (2012). Pathogenesis Related Proteins in Plant Defense Response. In: Plant Defence: Biological Control. Progress in Biological Control Vol 12. (Eds) Mérillon J, Ramawat K. ED Springer Dordrecht. Pp. 379-403. Doi: https://doi.org/10.1007/978-94-007-1933-0_17

Thomma BPHJ, Nürnebereger T, Joosten MHAJ. (2011). Of PAMPs and effectors: The blurred PTI-ETI Dichotomy. The Plant Cell. 23:4-15. Doi: https://doi.org/10.1105/tpc.110.082602

Tian MY, Win .J, Song J, van Der HR, van Der KE, Kamoun.S. (2016). A Phytophthora infestans cystatin-like protein targets a novel tomato papain-like apoplastic protease. Plant Physiol. 143:364-377. Doi: https://doi.org/10.1104/pp.106.090050

Tör M. (2008). Tapping into molecular conversation between oomycete plant pathogens and their hosts. Eur. J. Plant Pathol. 122:57-69. Doi: https://doi.org/10.1007/s10658-008-9288-z

Torto AT, Collmer CW, Lindeber M, Bird D, Collmer A, Tyler BM. (2009). Common and contrasting themes in host cell-targeted effectors from bacterial, fungal, oomycete and nematode plant symbionts described using the Gene Ontology. BMC Microbiol. 9:1-8. Doi: https://doi.org/10.1186/1471-2180-9-S1-S3

Ueeda M, Kubota M, Nishi K. (2006). Contribution of jasmonic acid to resistance against Phytophthora blight in Capsicum annuum cv. SCM334. Physiol. Mol. Plant. Pathol. 67:149-154. Doi: https://doi.org/10.1016/j.pmpp.2005.12.002

Veloso J, Díaz J. (2012). Fusarium oxysporum Fo47 confers protection Pepper plants against Verticillium dahlia and Phytophthora capsici, and induces the expression of defence genes. Plant Pathol. 61:281-188. Doi: https://doi.org/10.1111/j.1365-3059.2011.02516.x

Veloso J, García T, Bernal A, Díaz J. (2014). New bricks on the wall of induced resistance: salicylic acid receptors and transgenerational priming. Eur. J. Plant Pathol. 38:685-693. Doi: https://doi.org/10.1007/s10658-013-0350-0

Vidhyasekaran P. (2014). PAMP signaling in plant innate immunity: Signal perception and transduction. In: Signaling and communication in plants series number 21. Springer Science+Busines Media Dordrecht. Pp. 17-161. Doi: https://doi.org/10.1007/978-94-007-7426-1

Villar-Luna E, Reyes-Trejo B, Rojas-Martínez RI, Gómez-Rodríguez O, Hernández-Anguiano AM, Zavaleta-Mejía E. (2009). Respuesta hipersensitiva en follaje de chile CM-334 resistente a Phytophthora capsici infectado con Nacobus aberrans. Nematropica. 39:143-155. En línea: http://journals.fcla.edu/nematropica/article/viewFile/64475/62143

Villar-Luna E, Rojas-Martinez R, Reyes-Trejo B, Gómez-Rodríguez O, Zavaleta-Mejía E. (2017). Mevalonate pathway genes expressed in chilli CM334 inoculated with Phytophthora capsici and infected by Nacobbus aberrans and Meloidogyne enterolobii. Eur. J. Plant Pathol. 148:867-881. Doi: https://doi.org/10.1007/s10658-016-1142-0

Villar-Luna H, Reyes-Trejo B, Gómez-Rodríguez O, Villar-Luna E, Zavaleta-Mejía E. (2015) Expresión de genes de defensa y acumulación de capsidiol en la interacción compatible CM334/ Nacobus aberrans e incompatible CM334/Meloidogyne incognita. Nematropica 45:9-19. En línea: http://journals.fcla.edu/nematropica/article/view/85048/81977

Win J, Chaparro GA, Belhaj K, Saunders DG, Yoshida K, Dong S, Shornack S, Zipfel C, Robatzek S, Hogenhout SA, Kamoun S. (2012). Effector biology of plant-associated organisms: Concepts and perspectives. Cold Spring Harb Symp Quant. Biol. 77:235-47. Doi: http://dx.doi.org/10.1101/sqb.2012.77.015933

Xu S, Kim BS. (2016). Evaluation of Paenibacillus polymyxa strain SC09-21 for biocontrol of Phytophthora blight and growth stimulation in pepper plants. Trop. Plant Pathol. 41:62. Doi: https://doi.org/10.1007/s40858-016-0077-5

Yi SY, Lee DJ, Yeom SI, Yoon J, Kim YH, Kwon SY, Choi D. (2010). A novel pepper (Capsicum annuum) receptor-like kinase functions as a negative regulator of plant cell death via accumulation of superoxide anions. New Phytol. 185:701-705. Doi: https://doi.org/10.1111/j.1469-8137.2009.03095.x




DOI: http://dx.doi.org/10.18781/R.MEX.FIT.1901-3

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