Innate Immunity of Phlomis purpurea against Phytophthora cinnamomi: A Transcriptomic Analysis

Phlomis purpurea L. grows spontaneously in dry and stony habitats from the south of Iberian Peninsula and in cork oak (Quercus suber L.) and holm oak (Q. ilex ssp. rotundifolia, Lam.) plantations infested with Phytophthora cinnamomi (Rands). The aim of this study is to understand the genetic basis of P. purpurea innate immunity to this pathogen. The transcriptome analysis of   P. purpurea upon challenging with P. cinnamomi revealed a set of up-regulated genes, related to signaling, transcription factors and response to stress. Transcripts involved in the synthesis of a number of proteins, namely: ANKYRIN, AP2, AQUAPORIN, ARMADILLO, At1G69870-LIKE, BHLH, BON1, CALMODULIN, CALNEXIN, CALRETICULINE, CC-NBS-LRR, CHAPERONE, CYTOCHROME, DUF, GH3, GMP, G-TYPE, LIPOXYGENASE, MLO-LIKE, MYB, NAC, NBS-LRR, PENTATRICOPEPTIDE, SUBTILISIN, WAK, bZIP and hormones such as BRASSINOSTEROID, JASMONATE, SALICYLATE, ETHYLENE-RESPONSIVE were identified. P. purpurea ability to cope with P. cinnamomi attack is based on the expression of a set of transcription factors and signaling molecules targeted by the pathogen. The information gathered contributes to the elucidation of the overall response of     P. purpurea to P. cinnamomi attempted infection which can be helpful for improving woody species resistance to pathogenic oomycetes.

[1]   Malik, N. A. A., Kumar, I. S., and Nadarajah, K. 2020. “Elicitor and Receptor Molecules: Orchestrators of Plant Defense and Immunity.” Int. J. Mol. Sci. 21: 963. doi: 10.3390/ijms21030963.

[2]   Afzal, A. J., Wood, A. J., and Lightfoot, D. A. 2008. “Plant Receptor-Like Serine Threonine Kinases: Roles in Signaling and Plant Defense.” MPMI 21: 507-17. doi: 10.1094/MPMI-21-5-0507.

[3]   Sarris, P. F., Cevik, V., Dagdas, G., Jones, J. D. G., and Krasileva, K. V. 2016. “Comparative Analysis of Plant Immune Receptor Architectures Uncovers Host Proteins Likely Targeted by Pathogens.” BMC Biology 14. doi: 10.1186/s12915-016-0228-7.

[4]   Dodds, P. N., and Rathtjen, J. P. 2010. “Plant Immunity: Towards an Integrated View of Plant-Pathogen Interactions.” Nat Revi. Genet. 11: 539-48. doi: 10.1038/nrg2812.

[5]   Hammond-Kosack, K. E., and Jones, J. D. G. 1997. “Plant Disease Resistance Genes.” Annu. Rev. Plant Physiol. Plant Mol. Biol. 48: 575-607. doi: 10.1146/annurev.arplant.48.1.575.

[6]   Kushalappa, A. C., Yogendra, K. N., and Karre, S. 2016. “Plant Innate Immune Response: Qualitative and Quantitative Resistance.” Critical Reviews in Plant Sciences 35 (1): 38-55. doi: 10.1080/07352689.2016.1148980.

[7]   Muthamilarasan, M., and Prasad, M. 2013. “Plant Innate Immunity: An Updated Insight into Defense Mechanism.” J. Biosci. 38: 433-49. doi: 10.1007/s12038-013-9302-2.

[8]   Najafi, J., Brembu, T., Vie, A. K., Viste, R., Winge, P., Somssich, I. E., and Bones, A. M. 2020. “PAMP-INDUCED SECRETED PEPTIDE 3 Modulates Immunity in Arabidopsis.” J. Exp. Bot. 71: 850-64. doi: 10.1093/jxb/erz482.

[9]   Nuruzzaman, M., Sharoni, A. M., and Kikuchi, S. 2013. “Roles of NAC Transcription Factors in the Regulation of Biotic and Abiotic Stress Responses in Plants.” Front. Microb. 4: 248. doi: 10.3389/fmicb.2013.00248.

[10]  Lin, R., Zhaom, W., Mengm, X., Wang, M., and Peng, Y. 2007. “Rice gene OsNAC19 Encodes a Novel NAC-Domain Transcription Factor and Responds to Infection by Magnaporthe grisea.” Plant Sci. 172: 120-30. doi: 10.1016/j.plantsci.2006.07.019.

[11]  Liu, L.-P., Qu, J.-W., Yi, X.-Q., and Huang, H.-H. 2017. “Genome-Wide Identification, Classification and Expression Analysis of the Mildew Resistance Locus O (MLO) Gene Family in Sweet Orange (Citrus sinensis).” Braz. Arch. Biol. Technol. 60: e17160474. doi: 10.1590/1678-4324-2017160474.

[12]  Pessina, S., Lenzi, L., Perazzolli, M., Campa, M., Costa, L. D., Urso, S., Valè, G., Salamini, F., Velasco, R., and Malnoy, M. 2016. “Knockdown of MLO Genes Reduces Susceptibility to Powdery Mildew in Grapevine.” Hort. Res. 3: 16016. doi: 10.1038/hortres.2016.16.

[13]  Kunkel, B. N., and Brooks, D. M. 2002. “Cross Talk between Signaling Pathways in Pathogen Defense.” Curr. Opin. Plant Biol. 5: 325-31. doi: 10.1016/s1369-5266(02)00275-3.

[14]  Robertson, D. N. 2013. “Modulating Plant Calcium for Better Nutrition and Stress Tolerance.” ISRN Bot. 5, art. 952043. doi: 10.1155/2013/952043.

[15]  Delgado-Cerrone, L., Alvarez, A., Mena, E., Ponce de León, I., and Montesano, M. 2018. “Genomewide Analysis of the Soybean CRK-Family and Transcriptional Regulation by Biotic Stress Signals Triggering Plant Immunity.” PLoS ONE 13: 0207438. doi: 10.1371/journal. pone.0207438.

[16]  Duclos, J., Fauconnier, A., Coelho, A. C., Bollen, A., Cravador, A., and Godfroid, E. 1998. “Identification of an Elicitin Gene Cluster in Phytophthora cinnamomi.” DNA Sequence 9: 231-7. doi: 10.3109/10425179809105210.

[17]  Ebadzad, G., Medeira, C., Maia, I., Martins, J., and Cravador, A. 2015. “Induction of Defence Responses by Cinnamomins against Phytophthora cinnamomi in Quercus suber and Quercus ilex Subs. rotundifolia.” Eur. J. PlantPathol. 143: 705-23. doi: 10.1007/s10658-015-0721-9.

[18]  Neves, D., Caetano, P., Oliveira, J., Maia, C., Horta, M., Sousa, N., Salgado, M., Dionísio, L., Magan, N., and Cravador, A. 2014. “Anti-Phytophthora cinnamomi Activity of Phlomis purpurea Plant and Root Extracts.” Eur. J. Plant Pathol. 138: 835-46. doi: 10.1007/s10658-013-0357-6.

[19]  Mateus, M. C., Neves, D., Dacunha, B., Laczko, E., Maia, C., Teixeira, R., and Cravador, A. 2016. “Structure, Anti-Phytophthora and Anti-tumor Activities of a Nortriterpenoid from the Rhizome of Phlomis purpurea (Lamiaceae).” Phytochemistry 131: 158-64. doi: 10.1016/j.phytochem.2016.09.004.

[20]  Baldé, A., Neves, D., García-Breijo, F. J., Pais, M. S., and Cravador, A. 2017. “De Novo Assembly of Phlomis purpurea after Challenging with Phytophthora cinnamomi.” BMC Genomics 18: 700. doi: 10.1186/s12864-017-4042-6.

[21]  Byrt, P., and Grant, B. R. 1979. “Some Conditions Governing Zoospore Production in Axenic Cultures of Phytophthora cinnamomi Rands.” Aust. J. Bot. 27: 103-15. doi: 10.1071/bt9790103.

[22]  Ausubel, F. 2005. “Are Innate Immune Signaling Pathways in Plants and Animals Conserved?” Nat. Immunol. 6: 973-9. doi: 10.1038/ni1253.

[23]  Andersen, E. J., Ali, S., Byamukama, E., Yen, Y., and Nepal, M. P. 2018. “Disease Resistance Mechanisms in Plants.” Genes 9: 339. doi: 10.3390/genes9070339.

[24]  Brutus, A., and Yang He, S. 2010. “Broad-Spectrum Defence against Plant Pathogens.” Nat. Biotechnol. 28: 330-1. doi: 10.1038/nbt0410-330.

[25]  Wrzaczek, M., Brosché, M., Salojärvi, J., Kangasjärvi, S., Idänheimo, N., Mersmann, S., Robatzek, S., Karpiński, S., Karpińska, B., and Kangasjärvi, J. 2010. “Transcriptional Regulation of the CRK/DUF26 Group of Receptor-Like Protein Kinases by Ozone and Plant Hormones in Arabidopsis.” BMC Plant Biol. 10, art. 95. doi: 10.1186/1471-2229-10-95.

[26]  Greeff, C., Roux, M., Mundy, J., and Petersen, M. 2012. “Receptor-Like Kinase Complexes in Plant Innate Immunity.” Front. Plant Sci. 3, art. 209. doi: 10.3389/fpls.2012.00209.

[27]  Eckardt, N. 2017. “The Plant Cell Reviews Plant Immunity: Receptor-Like Kinases, ROS-RLK Crosstalk, Quantitative Resistance, and the Growth/Defence Tradeoff.” Plant Cell 29: 601-2. doi: 10.1105/tpc.17.00289.

[28]  Kanzaki, H., Saitoh, H., Takahashi, Y., Berberich, T., Ito, A., Kamoun, S., and Terauchi, R. 2008. “NbLRK1, a Lectin-Like Receptor Kinase Protein of Nicotiana benthamiana, Interacts with Phytophthora infestans INF1 Elicitin and Mediates INF1-Induced Cell Death.” Planta 228: 977-87. doi: 10.1007/s00425-008-0797-y.

[29]  Singh, P., and Zimmerli, L. 2013. “Lectin Receptor Kinases in Plant Innate Immunity.” Front. Plant Sci. 4, art. 124. doi: 10.3389/fpls.2013.00124.

[30]  Wang, Y., Cordewener, J. H. G., America, A. H. P., Shan, W., Bouwmeester, K., and Govers, F. 2015. “Arabidopsis Lectin Receptor Kinases LecRK-IX.1 and LecRK-IX.2 Are Functional Analogs in Regulating Phytophthora Resistance and Plant Cell Death.” MPMI 28: 1032-48. doi: 10.1094/MPMI-02-15-0025-R.

[31]  Wang, Y., and Bouwmeester, K. 2017. “L-Type Lectin Receptor Kinases: New Forces in Plant Immunity.” PLoS Pathog 13: e1006433. doi: 10.1371/journal.ppat.1006433E.

[32]  Muchero, W., Sondreli, K. L., Chen, J.-G., Urbanowicz, B. R., Zhang, J., Singan, V., Yang, Y., Brueggeman, R. S., Franco-Coronado, J., Abraham, N., Yang, J.-Y., Moremen, K. W., Weisberg, A. J., Chang, J. H., Lindquist, E., Barry, K., Ranjan, P., Jawdy, S., Schmutz, J., Tuskan, G. A., and LeBoldus, J. M. 2018. “Association Mapping, Transcriptomics, and Transient Expression Identify Candidate Genes Mediating Plant-Pathogen Interactions in a Tree.” Proc. Natl. Acad. Sci. U.S.A. 115: 11573-8. doi: 10.1073/pnas.1804428115.

[33]  He, Z. H., He, D., and Kohorn, B. D. 1998. “Requirement for the Induced Expression of a Cell Wall Associated Receptor Kinase for Survival during the Pathogen Response.” Plant J. 14: 55-63. doi: 10.1046/j.1365-313x.1998.00092.x.

[34]  Verica, J. A., and He, Z.-H. 2002. “The Cell Wall-Associated Kinase (WAK) and WAK-Like Kinase Gene Family.” Plant Physiol. 129: 455-9. doi: 10.1104/pp.011028.

[35]  Kohom, B. D., and Kohom, S. L. 2012. “The Cell Wall-Associated Kinases, WAKs, as Pectin Receptors.” Front. Plant Sci. 3, art. 88. doi:10.3389/fpls.2012.00088.

[36]  Schenk, P. M., Kazan, K., Wilson, I., Andersen, J. P., Richmond, T., Sommerville, S. C., and Manners, J. M. 2000. “Coordinated Plant Defence Responses in Arabidopsis Revealed by Microarray Analysis.” Proc. Natl. Acad. Sci. U.S.A. 97: 11655-60. doi: 10.1073/pnas.97.21.11655.

[37]  Delteil, A., Gobbato, E., Cayrol, B., Estevan, J., Michel-Romiti, C., Dievart, A., Kroj, T., and Morel, J.-B. 2016. “Several Wall-Associated Kinases Participate Positively and Negatively in Basal Defence against Rice Blast Fungus.” BMC Plant Biol. 16, art. 17. doi: 10.1186/s12870-016-0711-x.

[38]  Li, H., Zhou, S.-Y., Zhao, W.-S., Su, S.-C., and Peng, Y.-L. 2009. “A Novel Wall-Associated Receptor-Like Protein Kinase Gene, OsWAK1, Plays Important Roles in Rice Blast Disease Resistance.” Plant Mol. Biol. 69: 337-46. doi: 10.1007/s11103-008-9430-5.

[39]  Tanveer, T., Shaheen, K., Parveen, S., Kazi, A. G., and Ahmad, P. 2014. “Plant Secretomics.” Plant Signal. Behav. 9: 29426. doi: 10.4161/ psb.29426.

[40]  Yeh, Y.-H., Chang, Y.-H., Huang, P.-Y., Huang, J.-B., and Zimmerli, L. 2015. “Enhanced Arabidopsis Pattern-Triggered Immunity by Overexpression of Cysteine-Rich Receptor-Like Kinases.” Front. Plant Sci. 6, art. 322. doi: 10.3389/fpls.2015.00322.

[41]  Feng, W., Kita, D., Peaucelle, A., Cartwright, H. N., Doan, V., Duan, Q., Liu, M.-C., Maman, J., Steinhorst, L., Schmitz-Thom, I., Yvon, R., Kudla, J., Wu, H.-M., Cheung, A. Y., and Dinneny, J. R. 2018. “The FERONIA Receptor Kinase Maintains Cell-Wall Integrity during Salt Stress through Ca²⁺ Signaling.” Curr. Biol. 28: 666-75. doi: 10.1016/j.cub.2018.01.023.

[42]  Gronnier, J., Franck, C. M., Stegmann, M., DeFalco, T. A., Cifuentes, A. A., Dünser, K., Lin, W., Yang, Z., Kleine-Vehn, J., Ringli, C., and Zipfel, C. 2020. “FERONIA Regulates FLS2 Plasma Membrane Nanoscale Dynamics to Modulate Plant Immune Signaling.” bioRχiv. doi: 10.1101/2020.07.20.212233.

[43]  Trusov, Y., and Botella, J. R. 2016. “Plant G-Proteins Come of Age: Breaking the Bond with Animal   Models.” Front. Chem. 4: 24. doi: 10.3389/fchem.2016.00024.

[44]  Trusov, Y., and Botella, J. R. 2012. “New Faces in Plant Innate Immunity: Heterotrimeric G Proteins.” J. Plant Biochem. Biotechnol. 20: 40-7. doi: 10.1007/s13562-012-0140-3.

[45]  Phillips, S. M., Dubery, I. A., and Henriette van Heerden, H. 2012. “Molecular Characterization of an Elicitor-Responsive Armadillo Repeat Gene (GhARM) from Cotton (Gossypium hirsutum).” Mol. Biol. Rep. 39: 8513-23. doi: 10.1007/s11033-012-1706-9.

[46]  Kim, M. C., Panstruga, R., Elliott, C., Müller, J., Devoto, A., Yoon, H. W., Park, H. C, Cho, M. J., and Schulze-Lefert, P. 2002. “Calmodulin Interacts with MLO Protein to Regulate Defence against Mildew in Barley.” Nature 416: 447-50. doi: 10.1038/416447a.

[47]  Humphry, M., Bednarek, P., Kemmerling, B., Koh, S., Stein, M., Göbel, U., Stüber, K., Pislewska-Bednarek, M., Loraine, A., Schulze-Lefert, P., Somerville, S., and Panstruga, R. 2010. “A Regulon Conserved in Monocot and Dicot Plants Defines a Functional Module in Antifungal Plant Immunity.” Proc. Natl. Acad. Sci. U.S.A. 107: 21896-901. doi: 10.1073/pnas.1003619107.

[48]  Lewis, J. D., Wan, J., Ford, R., Gong, Y., Fung, P., Nahal, H., Wang, P. W., Desveaux, D., and Guttman, D. S. 2012. “Quantitative Interactor Screening with Next Generation Sequencing (QIS-Seq) Identifies Arabidopsis thaliana MLO2 as a Target of the Pseudomonas syringae Type III Effector HopZ2.” BMC Genomics 13, art. 8. doi: 1471-2164/13/8.

[49]  Lee, J.-H., Hye Sup Yun, H. S., and Kwon, C. 2012. “Molecular Communications between Plant Heat Shock Responses and Disease Resistance.” Mol. Cells 34: 109-16. doi: 10.1007/s10059-012-0121-3.

[50]  Kim, M. C., Lee, S. H., Kim, J. K., Chun, H. J., Choi, M. S., Woo Sik Chung, W. S., Moon, B. C., Kang, C. H., Park, C. Y., Yoo, J. H., Kang, Y. H., Koo, S. C., Koo, Y. D., Jung, J. C., Kim, S. T., Schulze-Lefert, P., Lee, S. Y., and Cho, M. J. 2002. “Mlo, a Modulator of Plant Defence and Cell Death, Is a Novel Calmodulin-Binding Protein.” J. Biol. Chem. 277: 19304-14. doi: 10.1074/jbc.M108478200.

[51]  Lalonde, S., Sero, A., Pratelli, R., Pilot, G., Chen, J., Sardi, M. I., Parsa, S. A., Kim, D.-Y., Biswa, R., Acharya, B. R., Stein, E. V., Hu, H.-C., Villiers, F., Takeda, K., Yang, Y., Han, Y. S., Schwacke, R., Chiang, W., Kato, N., Loqué, D., Assmann, S. M., Kwak, J. M., Schroeder, J. I., Rhee, S. Y., and Frommer, W. B. A. 2010. “Membrane Protein/Signaling Protein Interaction Network for Arabidopsis Version AMPv2.” Front. Physiol. 1, art. 24. doi: 10.3389/fphys.2010.00024.

[52]  Lyngkjær, M. F., and Carver, T. L. W. 2000. “Conditioning of Cellular Defence Responses to  Powdery Mildew in Cereal Leaves by Prior Attack.” Mol. Plant Pathol. 1: 41-9. doi: 10.1046/j.1364-3703.2000.00006.x.

[53]  Joshi, R., Wani, S. H., Singh, B., Bohra, A., Dar, Z. A., Lone, A. A., Pareek, A., and Singla-Pareek, S. L. 2016. “Transcription Factors and Plants Response to Drought Stress: Current Understanding and Future Directions.” Front. Plant Sci. 7, art. 1029. doi: 10.3389/fpls.2016.01029.

[54]  Matsukawa, M., Shibata, Y., Ohtsu, M., Mizutani, A., Mori, H., Wang, P., Ojika, M., Kawakita, K., and Takemoto, D. 2013. “Nicotiana benthamiana Calreticulin 3a Is Required for the Ethylene-Mediated Production of Phytoalexins and Disease Resistance against Oomycete Pathogen Phytophthora infestans.” MPMI 26: 880-92. doi: 10.1094/MPMI-12-12-0301-R.

[55]  Crofts, A. J., and Denecke, J. 1998. “Calreticulin and Calnexin in Plants.” Trends Plant Sci. 3: 396-9. doi: 10.1016/S13601385(98)013 12-0.

[56]  Tuteja, N., and Mahajan, S. 2007. “Calcium Signaling Network in Plants: An Overview.” Plant Signal. Behav. 2: 79-85. doi: 10.4161/psb.2.2.4176.

[57]  Gupta, D., and Tuteja, N. 2011. “Chaperones and Foldases in Endoplasmic Reticulum Stress Signaling in Plants.” Plant Signal. Behav. 6: 232-6. doi: 10.4161/psb.6.2.15490.

[58]  Sarwat, M., and Naqvi, A. R. 2013. “Heterologous Expression of Rice Calnexin (OsCNX) Confers Drought Tolerance in Nicotiana tabacum.” Mol. Biol. Rep. 40: 5451-64. doi: 10.1007/s11033-013-2643-y.

[59]  Yang, D. L., Shi, Z., Bao, Y., Yan, J., Yang, Z., Yu, H., Li, Y., Gou, M., Wang, S., Zou, B., Xu, D., Ma, Z., Kim, J., and Hua, J. 2017. “Calcium Pumps and Interacting BON1 Protein Modulate Calcium Signature, Stomatal Closure, and Plant Immunity.” Plant physiol. 175: 424-37. doi: 10.1104/pp.17.00495.

[60]  Kim, J, Lim, C. J., Lee, B. W., Choi, J. P., Oh, S. K., Ahmad, R., Kwon, S.-Y., Ahn, J., and Hur, C.-G. 2012. “A Genome-Wide Comparison of NB-LRR Type of Resistance Gene Analogs (RGA) in the Plant Kingdom.” Mol. Cells 33: 385-92. doi: 10.1007/s10059-012-0003-8.

[61]  Xu, Y., Liu, F., Zhu, S., and Li, X. 2018. “The Maize NBS-LRR Gene ZmNBS25 Enhances Disease Resistance in Rice and Arabidopsis.” Front. Plant Sci. 9, art. 1033. doi: 10.3389/fpls.2018.01033.

[62]  Hammond-Kosack, K. E., and Parker, J. E. 2003. “Deciphering Plant-Pathogen Communication: Fresh Perspectives for Molecular Resistance Breeding.” Curr. OpinBiotechnol. 14: 177-93. doi: 10.1016/s0958-1669(03)00035-1.

[63]  Pedley, K. F., and Martin, G. B. 2005. “Role of Mitogen-Activated Protein Kinases in Plant Immunity.” Curr. Opin. Biotechnol. 8: 541-7. doi: 10.1016/j.pbi.2005.07.006.

[64]  Wu, J., Zhu, J., Wang, L., and Wang, S. 2017. “Genome-Wide Association Study Identifies NBS-LRR-Encoding Genes Related with Anthracnose and Common Bacterial Blight in the Common Bean.” Front. Plant Sci. 8, art. 1398. doi: 10.3389/fpls.2017.01398.

[65]  Sagi, M. S., Deokar, A. A., and Tar’an, B. 2017. “Genetic Analysis of NBS-LRR Gene Family in Chickpea and Their Expression Profiles in Response to Ascochyta Blight Infection.” Front. Plant Sci. 8, art. 838. doi: 10.3389/fpls.2017.00838.

[66]  Liu, J., Liu, X., Dai, L., and Wang, G. 2007. “Recent Progress in Elucidating the Structure, Function and Evolution of Disease Resistance Genes in Plants.” J. Genet. Genomics 34: 765-76. doi: 10.1016/S1673-8527(07)60087-3.

[67]  Elmore, J. M., Lin, Z. J. D., and Coaker, G. 2011. “Plant NB-LRR Signaling: Upstreams and Downstreams.” Curr. Opin. Plant Biol. 14: 365-71. doi: 10.1016/j.pbi.2011.03.011.

[68]  Zhang, C., Chen, H., Cai, T., Deng, Y., Zhuang, R., Zhang, N., Zeng, Y., Zheng, Y., Tang, R., Pan, R., and Zhuang, W. 2017. “Overexpression of a Novel Peanut NBS-LRR Gene AhRRS5 Enhances Disease Resistance to Ralstonia solanacearum in Tobacco.” Plant Biotechnol. J. 15: 39-55. doi: 10.1111/pbi.12589.

[69]  Goyal, N., Bhatia, G., Sharma, S., Garewal, N., Upadhyay, A., Upadhyay, S. K., and Singh, K. 2020. “Genome-Wide Characterization Revealed Role of NBS-LRR Genes during Powdery Mildew Infection in Vitis vinifera.” Genomics 112: 312-22. doi: 10.1016/j.ygeno.2019.02.011.

[70]  Li, X., Zhang, Y., Yin, L., and Lu, J. 2016. “Overexpression of Pathogen-Induced Grapevine TIR-NB-LRR Gene VaRGA1 Enhances Disease Resistance and Drought and Salt Tolerance in Nicotiana benthamiana.” Protoplasma 254: 957-69. doi: 10.1007/s00709-016-1005-8.

[71]  Reddy, A., Lavanya, B., Thunugunta, T., Eguru, S., Reddy, D. C., and Lakshmana, R. 2019. “Isolation and Characterization of NBS-Encoding Disease Resistance Gene Analogs in Watermelon against Fusarium Wilt.” Curr. Sci. 117: 617-26. doi: 10.18520/cs/v117/i4/617-626.

[72]  Moffett, P., Farnham, G., Peart, J., and Baulcombe, D. C. 2002. “Interaction between Domains of a Plant NBS-LRR Protein in Disease Resistance-Related Cell Death.” EMBO J. 21: 4511-9. doi: 10.1093/emboj/cdf453.

[73]  Tian, S., Wang, X., Li, P., Wang, H., Ji, H., Xie, J., Qiu, Q., Shen, D., and Dong, H. 2016. “Plant Aquaporin AtPIP1; 4 Links Apoplastic H₂O₂ Induction to Disease Immunity Pathways.” Plant Physiol. 171: 1635-50. doi: 10.1104/pp.15.01237.

[74]  Zhang, L, Chen, L., and Dong, H. 2019. “Plant Aquaporins in Infection by and Immunity against Pathogens—A Critical Review.” Front. Plant Sci. 10, art. 632. doi: 10.3389/fpls.2019.00632.

[75]  Li, G., Chen, T., Zhang, Z., Li, B., and Tian, S. 2020. “Roles of Aquaporins in Plant-Pathogen Interaction.” Plants 9: 1134. doi: 10.3390/plants9091134.

[76]  Baillo, E. H., Kimotho, R. N., Zhang, Z., and Xu, P. 2019. “Transcription Factors Associated with Abiotic and Biotic Stress Tolerance and Their Potential for Crops Improvement.” Genes 10: 771. doi: 10.3390/genes10100771.

[77]  Javed, T., Shabbir, R., Ali, A., Afzal, I., Zaheer, U., and Gao, S.-J. 2020. “Transcription Factors in Plant Stress Responses: Challenges and Potential for Sugarcane Improvement.” Plants 9: 491. doi: 10.3390/plants9040491.

[78]  Nakashima, K., Yamaguchi-Shinozaki, K., and Shinozaki, K. 2014. “The Transcriptional Regulatory Network in  the Drought Response and Its Cross Talk in Abiotic Stress Responses Including Drought, Cold, and Heat.” Front. Plant Sci. 5, art. 170. doi: 10.3389/fpls.2014.00170.

[79]  Yuan, X., Wang, H., Cai, J., Li, D., and Song, F. 2019. “NAC Transcription Factors in Plant Immunity.” Phytopathol. Res. 1, art. 3. doi: 10.1186/s42483-018-0008-0.

[80]  Hichri, I., Barrieu, F., Bogs, J., Kappel, C., Delrot, S., and Lauvergeat, V. 2011. “Recent Advances in the Transcriptional Regulation of the Flavonoid Biosynthetic Pathway.” J. Exp. Bot. 62: 2465-83. doi: 10.1093/jxb/erq442.

[81]  Ambawat, S., Sharma, P., Yadav, N. R., and Yadav, R. C. 2013. “MYB Transcription Factor Genes as Regulators for Plant Responses: An Overview.” Physiol. Mol. Biol. Plants 19: 307-21. doi: 10.1007/s12298-013-0179-1.

[82]  Roy, S. 2016. “Function of MYB Domain Transcription Factors in Abiotic Stress and Epigenetic Control of Stress Response in Plant Genome.” Plant Signal. Behav. 11: e1117723. doi: 10.1080/15592324.2015.1117723.

[83]  Mengiste, T., Chen, X., Salmeron, J., and Dietrich, R. 2003. “The BOTRYTIS SUSCEPTIBLE1 Gene Encodes an R2R3MYB Transcription Factor Protein That Is Required for Biotic and Abiotic Stress Responses in Arabidopsis.” Plant Cell 15: 2551-65. doi: 10.1105/tpc.014167.

[84]  Noman, A., Hussain, A., Adnan, M., Khan M. I., Ashraf, M. F., Zainab, M., Khan, K. A., Ghramh, H. A., and He, S. 2019. “A Novel MYB Transcription Factor CaPHL8 Provide Clues about Evolution of Pepper Immunity against Soil Borne Pathogen.” Microb. Pathog. 137: 103758. doi: 10.1016/j.micpath.2019.103758.

[85]  Feller, A., Machemer, K., Braun, E. L., and Grotewold, E. 2011. “Evolutionary and Comparative Analysis of MYB and bHLH Plant Transcription Factors.” Plant J. 66: 94-116. doi: 10.1111/j.1365-313X.2010.04459.x.

[86]  Xu, F., Kapos, P., Cheng, Y. T., Li, M., Zhang, Y., and Li, X. 2014. “NLR-Associating Transcription Factor bHLH84 and Its Paralogs Function Redundantly in Plant Immunity.” PLoS Pathog 10: e1004312. doi: 10.1371/journal.ppat.1004312.

[87]  Wei, K., Chen, J., Wang, Y., Chen, Y., Chen, S., Lin, Y., Pan, S., Zhong, X., and Xie, D. 2012. “Genome-Wide Analysis of bZIP-Encoding Genes in Maize.” DNA Res. 19: 463-76. doi: 10.1093/dnares/dss026.

[88]  Jakoby, M., Weisshaar, B., Dröge-Laser, W., Vicente-Carbajosa, J., Tiedemann, J., Kroj, T., and Parcy, F. 2002. “bZIP Transcription Factors in Arabidopsis.” Trends Plant Sci. 7: 106-11. doi: 10.1016/S1360-1385(01)02223-3.

[89]  Alves, M. S., Dadalto, S. P., Gonçalves, A. B., De Souza, G. B., Barros, V. A., and Fietto, L. G. 2013. “Plant bZIP Transcription Factors Responsive to Pathogens: A Review.” Int. J. Mol. Sci. 14: 7815-28. doi: 10.3390/ijms14047815.

[90]  Liu, D., Shi, S., Hao, Z., Xiong, W., and Luo, M. 2019. “OsbZIP81, a Homologue of Arabidopsis VIP1, May Positively Regulate JA Levels by Directly Targetting the Genes in JA Signaling and Metabolism Pathway in Rice.” Int. J. Mol. Sci. 20: 2360. doi: 10.3390/ijms20092360.

[91]  Vo, K. T. X., Kim, C.-Y., Chandran, A. K. N., Jung, K.-H., An, G., and Jeon, J.-S. 2015. “Molecular Insights into the Function of Ankyrin Proteins in Plants.” J. Plant Biol. 58: 271-84. doi: 10.1007/s12374-015-0228-0.

[92]  Kazan, K., and Lyons, R. 2014. “Intervention of Phytohormone Pathways by Pathogen Effectors.” Plant Cell 26: 2285-309. doi: 10.1105/tpc.114.125419.

[93]  Pieterse, C. M. J., Van der Does, D., Zamioudis, C., Leon-Reyes, A., and Van Wees, S. C. M. 2012. “Hormonal Modulation of Plant Immunity.” Annu. Rev. Cell Dev. Biol. 28: 489-521. doi: 10.1146/annurev-cellbio-092910-154055.

[94]  Hardham, A. R., and Blackman, L. M. 2018. “Phytophthora cinnamomi.” Mol. Plant Pathol. 19: 260-85. doi: 10.1111/mpp.12568.

[95]  Epple, P., Apel, K., and Bohlmann, H. 1997. “ESTs Reveal a Multigene Family for Plant Defensins in Arabidopsis thaliana.” FEBS J. 400: 168-72. doi: 10.1016/S0014-5793(96)01378-6.

[96]  Glazebrook, J. 2005. “Contrasting Mechanisms of Defence against Biotrophic and Necrotrophic Pathogens.” Annu. Rev. Phytopathol. 43: 205-27. doi: 10.1146/annurev.phyto.43.040204.135923.

[97] Contreras-Cornejo, H. A., Macías-Rodríguez, L., Beltrán-Peña, E., Herrera-Estrella, A., and López-Bucio, J. 2011. “Trichoderma-Induced Plant Immunity Likely Involves Both Hormonal- and Camalexin-Dependent Mechanisms in Arabidopsis thaliana and Confers Resistance against Necrotrophic Fungi Botrytis cinerea.” Plant Signal. Behav. 6: 1554-63. doi: 10.4161/psb.6.10.17443.

[98] Di, X., Gomila, J., and Takken, F. L. W. 2017. “Involvement of Salicylic Acid, Ethylene and Jasmonic Acid Signalling Pathways in the Susceptibility of Tomato to Fusarium oxysporum.” Mol. PlantPathol. 18: 1024-35. doi: 10.1111/mpp.12559.

[99] Guerreiro, A., Figueiredo, J., Sousa Silva, M., and Figueiredo, A. 2016. “Linking Jasmonic Acid to Grapevine Resistance against the Biotrophic Oomycete Plasmopara viticola.” Front. Plant Sci. 7, art. 565. doi: 10.3389/fpls.2016.00565.

[100] Guo, H., Nolan, T. M., Song, G., Liu, S., Xie, Z., Chen, J., Schnable, P. S., Walley, J. W., and Yin, Y. 2018. “FERONIA Receptor Kinase Contributes to Plant Immunity by Suppressing Jasmonic Acid Signaling in Arabidopsis thaliana.” Curr. Biol. 28: 3316-24. doi: 10.1016/j.cub.2018.07.078.

[101] Cao, F. Y., DeFalco, T. A., Moeder, W., Li, B., Gong, Y., Liu, X.-M., Taniguchi, M., Lumba, S., Toh, S., Shan, L., Ellis, B., Desveaux, D., and Yoshioka, K. 2018. “Arabidopsis ETHYLENE RESPONSE FACTOR 8 (ERF8) Has Dual Functions in ABA Signaling and Immunity.” BMC Plant Biol. 18, art. 211. doi: 10.1186/s12870-018-1402-6.

[102] McGrath, K. C., Dombrecht, B., Manners, J. M., Schenk, P. M., Edgar, C. I., Maclean, D. J., Scheible, W.-R., Udvardi, M. K., and Kazan, K. 2005. “Repressor and Activator-Type Ethylene Response Factors Functioning in Jasmonate Signaling and Disease Resistance Identified via a Genome-Wide Screen of Arabidopsis Transcription Factor Gene Expression.” Plant Physiol. 139: 949-59. doi: 10.1104/pp.105.068544.

[103] Huang, P.-Y., Catinot, J., and Zimmerli, L. 2016. “Ethylene Response Factors in Arabidopsis Immunity.” J. Exp. Bot. 67: 1231-41. doi:10.1093/jxb/erv518.

[104] Li, C.-W., Su, R.-C., Cheng, C.-P., Sanjaya, Y. S.-J., Hsieh, T.-H., and Chao, T.-C. M.-T. 2011. “Tomato  RAV Transcription Factor Is a Pivotal Modulator Involved in the AP2/EREBP-Mediated Defense  Pathway.” Plant Physiol. 156: 213-27. doi: 10.1104/pp.111.174268.

[105] Thirugnanasambantham, K., Durairaj, S., Saravanan, S., Karikalan, K., Muralidaran, S., and Islam, V. I. H. 2015. “Role of Ethylene Response Transcription Factor (ERF) and Its Regulation in Response to Stress Encountered by Plants.” Plant Mol. Biol. Rep. 33: 347-57. doi: 10.1007/s11105-014-0799-9.

[106] Zhang, C., Gao, H., Li, R., Han, D., Wang, L., Wu, J., Xu, P., and Zhang, S. 2019. “GmBTB/POZ, a Novel BTB/POZ Domain-Containing Nuclear Protein, Positively Regulates the Response of Soybean to Phytophthora sojae Infection.” Mol. Plant Pathol. 20: 78-91. doi: 10.1111/mpp.12741.

[107] Corratgé-Faillie, C., and Lacombe, B. 2017. “Substrate (Un)specificity of Arabidopsis NRT1/PTR FAMILY (NPF) Proteins.” J. Exp. Bot. 68: 3107-13. doi: 10.1093/jxb/erw499.

[108] Isner, J. C., Nühse, T., and Maathuis, F. J. M. 2012. “The Cyclic Nucleotide cGMP Is Involved in Plant Hormone Signalling and Alters Phosphorylation of Arabidopsis thaliana Root Proteins.” J. Exp. Bot. 63: 3199-205. doi: 10.1093/jxb/ers045.

[109] Westfall, C. S., Sherp, A. M., Zubieta, C., Alvarez, S., Schraft, E., Marcellin, R., Ramirez, L., and Jez, J. M. 2016. “Arabidopsis thaliana GH3.5 Acyl Acid    Amido Synthetase Mediates Metabolic Crosstalk in Auxin and Salicylic Acid Homeostasis.” Proc. Natl. Acad. Sci. U.S.A. 113: 13917-22. doi: 10.1073/pnas.1612635113.

[110] Zou, X., Long, J., Zhao, K., Peng, A., Chen, M., Long, Q., Yongrui, H., and Shanchun, C. 2019. “Overexpressing GH3.1 and GH3.1L Reduces Susceptibility to Xanthomonas citri Subsp. citri by Repressing      Auxin Signaling in Citrus (Citrus sinensis Osbeck).” PLoS ONE 14: e0220017. doi: 10.1371/journal.pone.0220017.

[111] Huot, B., Yao, J., Montgomery, B. L., and He, S. Y. 2014. “Growth-Defense Tradeoffs in Plants: A Balancing Act to Optimize Fitness.” Mol. Plant 7: 1267-87. doi: 10.1093/mp/ssu049.

[112] Ahmad, F., Singh, A., and Kamal, A. 2018. “Crosstalk of Brassinosteroids with Other Phytohormones under Various Abiotic Stresses.” J. Appl. Biol. Biotechnol. 6: 56-62. doi: 10.7324/JABB.2018.60110.

[113] Vera, P., and Cornejero, V. 1988. “Pathogenesis-Related Proteins of Tomato-P 69 as an Alkaline Endoproteinase.” Plant Physiol. 87: 58-63. doi: 10.1104/pp.87.1.58.

[114] Schaller, A., Stintzi, A., and Graff, L. 2012. “Subtilases-Versatile Tools for Protein Turnover, Plant Development, and Interactions with the Environment.” Physiol. Plant 145: 52-66. doi: 10.1111/j.1399-3054.2011.01529.x.

[115] Ramírez, V., López, A., Mauch-Mani, B., Gil, M. J., and Vera, P. 2013. “An Extracellular Subtilase Switch for Immune Priming in Arabidopsis.” PLoS Pathog. 9: e1003445. doi: 10.1371 /journal. ppat.1003445.

[116] Figueiredo, A., Monteiro, F., and Sebastiana, M. 2014. “Subtilisin-Like Proteases in Plant-Pathogen Recognition and Immune Priming: A Perspective.” Front. Plant Sci. 5, art. 739. doi: 10.3389/fpls.2014.00739.

[117] Wang, S., Xing, R., Wang, Y., Shu, H., Fu, S., Paulus, J. K., Schuster, M., Saunders, D. G. O., Win, J., Vleeshouwers, V., Zheng, X., van der Hoorn, R. A. L., Kamoun, S., and Dong, S. 2019. “Cleavage of a Pathogen Apoplastic Protein by Plant Subtilases Activates Immunity.” bioRχiv. doi: 10.1101/ 2019.12.16.878272.

[118] Xu, J., Wang, X.-Y., and Guo, W.-Z. 2015. “The Cytochrome P450 Superfamily: Key Players in Plant Development and Defence.” J. Integr. Agric. 14: 1673-86. doi: 10.1016/S2095-3119(14)60980-1.

[119] Park, J. H., Halitschke, R., Kim, H. B., Baldwin, I. T., Feldmann, K. A., and Feyereisen, R. 2002. “A Knock-Out Mutation in Allene Oxide Synthase Results in Male Sterility and Defective Wound Signal Transduction in Arabidopsis due to a Block in Jasmonic Acid Biosynthesis.” Plant J. 31: 1-12. doi: 10.1046/j.1365-313x.2002.01328.x.

[120] Pandian, B. A., Sathishraj, R., Djanaguiraman, M., Prasad, P. V., and Jugulam, M. 2020. “Role of Cytochrome P450 Enzymes in Plant Stress Response.” Antioxidants 9: 454. doi: 10.3390/antiox9050454.

[121] Yan, Q., Cui, X., Lin, S., Gan, S., Xing, H., and Dou, D. 2016. “GmCYP82A3: A Soybean Cytochrome p450 Family Gene Involved in the Jasmonic Acid and Ethylene Signaling Pathway, Enhances Plant Resistance to Biotic and Abiotic Stresses.” PLoS ONE 11: e0162253. doi: 10.1371/journal.pone.0162253.

[122] Barkan, A., and Small, I. 2014. “Pentatricopeptide Repeat Proteins in Plants.” Annu. Rev. Plant Biol. 65: 415-42. doi: 10.1146/annurev-arplant-050213-040159.

[123] Xing, H., Fu, X., Yang, C., Tang, X., Guo, L., Li, C., Xu, C., and Luo, K. 2018. “Genome-Wide Investigation of Pentatricopeptide Repeat Gene Family in Poplar and Their Expression Analysis in Response to Biotic and Abiotic Stresses.” Sci. Rep. 8, art. 2817. doi: 10.1038/s41598-018-21269-1.

[124] Lee, K., Park, S. J., Han, J. H., Jeon, Y., Paiv, H.-S., and Kang, H. 2019. “A Chloroplast-Targeted Pentatricopeptide Repeat Protein PPR287 Is Crucial for Chloroplast Function and Arabidopsis Development.” BMC Plant Biol. 19, art. 244. doi: 10.1186/s12870-019-1857-0.

[125] Monaghan, J., and Li, X. 2010. “The HEAT Repeat Protein ILITYHIA Is Required for Plant Immunity.” Plant Cell Physiol. 51: 742-53. doi: 10.1093/pcp/pcq038.

[126] Sharma, M., and Pandey, G. K. 2016. “Expansion and Function of Repeat Domain Proteins during Stress and Development in Plants.” Front. Plant Sci. 6, art. 1218. doi: 10.3389/fpls.2015.01218.

[127] Feschotte, C., Jiang, N., and Wessler, S. R. 2002. “Plant Transposable Elements: Where Genetics Meets Genomics.” Nat. Rev. Genet. 3: 329-41. doi: 10.1038/nrg793.

[128] McClintock, B. 1984. “The Significance of Responses of the Genome to Challenge.” Science 226: 792-801. doi: 10.1126/science.15739260.

[129] Grandbastien, M.-A. 1998. “Activation of Plant Retrotransposons under Stress Conditions.” Trends in Plant Sci. 3: 181-7. doi: 10.1016/S1360-1385(98)01232-1.

[130] Bonchev, G. N. 2016. “Useful Parasites: The Evolutionary Biology and Biotechnology Applications of Transposable Elements.” J. Genet. 95: 1039-52. doi: 10.1007/s12041-016-0702-6.

[131] Lai, Y., and Eulgem, T. 2018. “Transcript-Level Expression Control of Plant NLR Genes.” Mol. Plant Pathol. 19: 1267-81. doi: 10.1111/mpp.12607.

[132] Zervudacki, J., Yu, A., Amesefe, D., Wang, J., Drouaud, J., Navarro, L., and Deleris, A. 2018. “Transcriptional Control and Exploitation of an Immune-Responsive Family of Plant Retrotransposons.” EMBO J. 37: e98482. doi: 10.15252/embj.201798482.

[133] Pouteau, S., Grandbastien, M.-A., and Boccara, M. 1994. “Microbial Elicitors of Plant Defence Responses Activate Transcription of a Retrotransposon.” Plant J. 5: 535-42. doi: 10.1046/j.1365-313X.1994.05040535.x.