Functional interplay of genes in prioritizing the responses of rice plants to fungal infection and abiotic stress

  • C. B. Sruthilaxmi
  • Subramanian Babu


Main conclusion

Based on severity and life threatening status, rice plants prioritize their molecular response to abiotic stress and fungal infection through switching-on and -off the cross-talking genes.


Rice (Oryza sativa L.) is a crop which is cultivated in diverse soil and agro-climatic conditions across the world. Major limiting factor in rice production is the impact of various biotic and abiotic stresses. Under field conditions, as like any other plant species, rice crop would encounter more than one stress and acclimate to grow by regulating its molecular and cellular responses. Plants are known to switch their responses using convergent nodes of cross-talking signaling pathways during simultaneous multiple stresses. If plants encounter different stress one after the other, predisposing to susceptibility or tolerance is likely to occur due to the overlapping genes and their protein products in different biotic and abiotic stresses. Several studies on individual genes as well as genome-wide analysis of responses of rice to fungal and abiotic stress have indicated up-regulation of transcription factors, pathogenesis-related proteins, antioxidants and related proteins, hormone responsive proteins, ribosome-inactivating proteins, hybrid proline-rich proteins, lectins and heme activator proteins. Although differences in expression level of these cross-talking genes have been observed, molecular and cellular mechanism mediated by them to simultaneously alleviate fungal infection and abiotic stress is largely unknown. The objective of this review is to relate the function of genes and proteins under abiotic stress conditions from the point of view of fungal infection to further our understanding of cross-talk interface. Creating a fungal–abiotic stress response cross-talk blueprint of genes and proteins in rice is required to develop multiple stress tolerant varieties.


Abiotic Biotic Cross-talk Rice Stress 



The authors sincerely acknowledge the support rendered by VIT University, Vellore in carrying out our research.

Compliance with ethical standards

Conflict of interest

The authors declare that there is no conflict of interests.

Research involving human participants and/or animals

The research work does not involve human participants and/or animals.

Informed consent

The research work does not involve human participants and hence informed consent does not arise.


  1. Agarwal P, Bhatt V, Singh R, Das M, Sopory SK, Chikara J (2013) Pathogenesis-related gene, JcPR-10a from Jatropha curcas exhibit RNase and antifungal activity. Mol Biotechnol 54:412–425CrossRefPubMedGoogle Scholar
  2. Agrawal GK, Rakwal R, Tamogami S, Yonekura M, Kubo A, Saji H (2002) Chitosan activates defense/stress response(s) in the leaves of Oryza sativa seedlings. Plant Physiol Biochem 40:1061–1069CrossRefGoogle Scholar
  3. Al Atalah B, De Vleesschauwer D, Xu J, Fouquaert E, Hofte M, Van Damme EJ (2014) Transcriptional behavior of EUL-related rice lectins toward important abiotic and biotic stresses. J Plant Physiol 171:986–992CrossRefPubMedGoogle Scholar
  4. Alam MdM, Tanaka T, Nakamura H, Ichikawa H, Kobayashi K, Yaeno T, Yamaoka N, Shimomoto K, Takayama K, Nishina H, Nishiguchi M (2014) Overexpression of a rice heme activator protein gene (OsHAP2E) confers resistance to pathogens, salinity and drought, and increases photosynthesis and tiller number. Plant Biotechnol J 13:85–96CrossRefPubMedGoogle Scholar
  5. Alam MdM, Nakamura H, Ichikawa H, Kobayashi K, Yaeno T, Yamaoka N, Nishiquchi M (2015) Overexpression of OsHAP2E for a CCAAT-binding factor confers resistance to Cucumber mosaic virus and Rice necrosis mosaic virus. J Gen Plant Pathol 81:32–41CrossRefGoogle Scholar
  6. Arlorio M, Ludwig A, Boller T, Bonfante P (1992) Inhibition of fungal growth by plant chitinases and β-1,3-glucanases. Protoplasma 171:34–43CrossRefGoogle Scholar
  7. Asano T, Hayashi N, Kobayashi M, Aoki N, Miyao A, Mitsuhara I, Ichikawa H, Komatsu S, Hirochika H, Kikuchi S, Ohsugi R (2012) A rice calcium-dependent protein kinase OsCPK12 oppositely modulates salt-stress tolerance and blast disease resistance. Plant J 69:26–36CrossRefPubMedGoogle Scholar
  8. Bieri S, Potrykus I, Futterer J (2000) Expression of active barley seed ribosome-inactivating protein in transgenic wheat. Theor Appl Genet 100:755–763CrossRefGoogle Scholar
  9. Cao Y, Song F, Goodman RM, Zheng Z (2006) Molecular characterization of four rice genes encoding ethylene-responsive transcriptional factors and their expressions in response to biotic and abiotic stress. J Plant Physiol 163:1167–1178CrossRefPubMedGoogle Scholar
  10. Chopra R, Saini R (2014) Transformation of blackgram (Vigna mungo (L.) Hepper) by barley chitinase and ribosome-inactivating protein genes towards improving resistance to Corynespora leaf spot fungal disease. Appl Biochem Biotechnol 174:2791–2800CrossRefPubMedGoogle Scholar
  11. Collinge DB, Kragh KM, Mikkelsen JD, Nielsen KK, Rasmussen U, Vad K (1993) Plant chitinases. Plant J 3:31–40CrossRefPubMedGoogle Scholar
  12. Corrado G, Bovi PD, Ciliento R, Gaudio L, Di Maro A, Aceto S, Lorito M, Rao R (2005) Inducible expression of a Phytolacca heterotepala ribosome-inactivating protein leads to enhanced resistance against major fungal pathogens in tobacco. Phytopathology 95:206–215CrossRefPubMedGoogle Scholar
  13. Deutch CE, Winicov I (1995) Post-transcriptional regulation of a salt-inducible alfalfa gene encoding a putative chimeric proline-rich cell wall protein. Plant Mol Biol 27:411–418CrossRefPubMedGoogle Scholar
  14. Di R, Tumer NE (2015) Pokeweed antiviral protein: its cytotoxicity mechanism and applications in plant disease resistance. Toxins 7:755–772CrossRefPubMedPubMedCentralGoogle Scholar
  15. Dixon DP, Lapthorn A, Edwards R (2002) Plant glutathione transferases. Genome Biol 3:Reviews3004 (Epub 26 Feb 2002) CrossRefPubMedPubMedCentralGoogle Scholar
  16. Dvorakova L, Cvrckova F, Fischer L (2007) Analysis of the hybrid proline-rich protein families from seven plant species suggests rapid diversification of their sequences and expression patterns. BMC Genom 12:412CrossRefGoogle Scholar
  17. Dvorakova L, Srba M, Opatrny Z, Fischer L (2012) Hybrid proline-rich proteins: novel players in plant cell elongation? Ann Bot 109:453–462CrossRefPubMedGoogle Scholar
  18. Edwards R, Dixon DP (2005) Plant glutathione transferases. Methods Enzymol 401:169–186CrossRefPubMedGoogle Scholar
  19. Gill SS, Tuteja N (2010) Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol Biochem 48:909–930CrossRefPubMedGoogle Scholar
  20. Goto S, Sasakura-Shimoda F, Suetsugu M, Selvaraj MG, Hayashi N, Yamazaki M, Ishitani M, Shimono M, Sugano S, Matsushita A, Tanabata T, Takatsuji H (2015) Development of disease-resistant rice by optimized expression of WRKY45. Plant Biotechnol J 13:753–765CrossRefPubMedGoogle Scholar
  21. Hamberger B, Ellis M, Friedmann M, Souza CA, Barbazuk B, Douglas CJ (2008) Genome-wide analyses of phenylpropanoid-related genes in Populus trichocarpa, Arabidopsis thaliana, and Oryza sativa: the Populus lignin toolbox and conservation and diversification of angiosperm gene families. Can J Bot 85:1182–1201CrossRefGoogle Scholar
  22. Hashimoto M, Kisseleva L, Sawa S, Furukawa T, Komatsu S, Koshiba T (2004) A novel rice PR10 protein, RSOsPR10, specifically induced in roots by biotic and abiotic stresses, possibly via the jasmonic acid signaling pathway. Plant Cell Physiol 45:550–559CrossRefPubMedGoogle Scholar
  23. Helliwell EE, Wang Q, Yang Y (2013) Transgenic rice with inducible ethylene production exhibits broad-spectrum disease resistance to the fungal pathogens Magnaporthe oryzae and Rhizoctonia solani. Plant Biotechnol J 11:33–42CrossRefPubMedGoogle Scholar
  24. Jach G, Gornhardt B, Mundy J, Logemann J, Pinsdorf E, Leah R, Schell J, Maas C (1995) Enhanced quantitative resistance against fungal disease by combinatorial expression of different barley antifungal proteins in transgenic tobacco. Plant J 8:97–109CrossRefPubMedGoogle Scholar
  25. Jain M, Ghanashyam C, Bhattacharjee A (2010) Comprehensive expression analysis suggests overlapping and specific roles of rice glutathione S-transferase genes during development and stress responses. BMC Genom 11:73CrossRefGoogle Scholar
  26. Jiang SY, Ramamoorthy R, Bhalla R, Luan HF, Venkatesh PN, Cai M, Ramachandran S (2008) Genome-wise survey of the RIP domain family in Oryza sativa and their expression profiles under various abiotic and biotic stresses. Plant Mol Biol 67:603–614CrossRefPubMedGoogle Scholar
  27. Jiang CJ, Shimono M, Sugano S, Kojima M, Yazawa K, Yoshida R, Inoue H, Hayashi N, Sakakibara H, Takatsuji H (2010) Abscisic acid interacts antagonistically with salicylic acid signaling pathway in rice-Magnaporthe grisea interaction. Mol Plant Microbe Interact 23:791–798CrossRefPubMedGoogle Scholar
  28. Jiang SY, Bhalla R, Ramamoorthy R, Luan HF, Venkatesh PN, Cai M, Ramachandran S (2012) Over-expression of OsRIP18 increases drought and salt tolerance in transgenic rice plants. Transgenic Res 21:785–795CrossRefPubMedGoogle Scholar
  29. Kim KY, Park SW, Chung YS, Chung CH, Kim JI, Lee JH (2004) Molecular cloning of low-temperature-inducible ribosomal proteins from soybean. J Exp Bot 55:1153–1155CrossRefPubMedGoogle Scholar
  30. Kim ST, Yu S, Kang YH, Kim SG, Kim JY, Kim SH, Kang KY (2008) The rice pathogen-related protein 10 (JIOsPR10) is induced by abiotic and biotic stresses and exhibits ribonuclease activity. Plant Cell Rep 27:593–603CrossRefPubMedGoogle Scholar
  31. Lillo C, Lea US, Ruoff P (2008) Nutrient depletion as a key factor for manipulating gene expression and product formation in different branches of the flavonoid pathway. Plant Cell Environ 31:587–601CrossRefPubMedGoogle Scholar
  32. Liu H, Zhang H, Yang Y, Li G, Yang Y, Wang X, Basnayake BM, Li D, Song F (2008) Functional analysis reveals pleiotropic effects of rice RING-H2 finger protein gene OsBIRF1 on regulation of growth and defense responses against abiotic and biotic stresses. Plant Mol Biol 68:17–30CrossRefPubMedGoogle Scholar
  33. Lyzenga WJ, Stone SL (2012) Abiotic stress tolerance mediated by protein ubiquitination. J Exp Bot 63:599–616CrossRefPubMedGoogle Scholar
  34. Maddaloni M, Forlani F, Balmas V, Donini G, Stasse L, Corazza L, Motto M (1997) Tolerance to the fungal pathogen Rhizoctonia solani AG4 of transgenic tobacco expressing the maize ribosome-inactivating protein b-32. Transgenic Res 6:393–402CrossRefGoogle Scholar
  35. Mellacheruvu S, Tamirisa S, Vudem DR, Khareedu VR (2016) Pigeonpea hybrid-proline-rice protein (CcHyPRP) confers biotic and abiotic stress tolerance in transgenic rice. Front Plant Sci 6:1167CrossRefPubMedPubMedCentralGoogle Scholar
  36. Moons A, Prinsen E, Bauw G, Montagu MV (1997) Antagonistic effects of abscisic acid and jasmonates on salt stress-inducible transcripts in rice roots. Plant Cell 9:2243–2259CrossRefPubMedPubMedCentralGoogle Scholar
  37. Nakashima K, Tran L-SP, Nguyen DV, Fujita M, Maruyama M, Todaka D, Ito Y, Hayashi N, Shinozaki K, Yamaguchi-Shimozaki K (2007) Functional analysis of a NAC-type transcription factor OsNAC6 involved in abiotic and biotic stress-responsive gene expression in rice. Plant J 51:617–630CrossRefPubMedGoogle Scholar
  38. Nakashima K, Takasaki H, Mizoi J, Shinoaki K, Yamaguchi-Shinozaki K (2012) NAC transcription factors in plant abiotic stress responses. Biochim Biophys Acta 1819:97–103CrossRefPubMedGoogle Scholar
  39. Narsai R, Ivanova A, Ng S, Whelan J (2010) Defining reference genes in Oryza sativa using organ, development, biotic and abiotic transcriptome datasets. BMC Plant Biol 10:56CrossRefPubMedPubMedCentralGoogle Scholar
  40. Narsai R, Wang C, Chen J, Wu J, Shou H, Whelan J (2013) Antagonistic, overlapping and distinct response to biotic stress in rice (Oryza sativa) and interactions with abiotic stress. BMC Genom 14:93CrossRefGoogle Scholar
  41. Park CH, Chen S, shirsekar G, Zhou B, Khang CH, Songkumarn P, Afzal AJ, Ning Y, Wang R, Bellizi M, Valent B, Wang GL (2012) The Magnaporthe oryzae effector AvrPiz-t targets the RING E3 ubiquitin ligase APIP6 to suppress pathogen-associated molecular pattern-triggered immunity in rice. Plant Cell 24:4748–4762CrossRefPubMedPubMedCentralGoogle Scholar
  42. Peng X-X, Tang X-K, Zhou P-L, Hu Y-J, Deng X-B, He Y, Wang H (2011) Isolation and expression patterns of rice WRKY82 transcription factor gene responsive to both biotic and abiotic stresses. Agr Sci China 10:893–901CrossRefGoogle Scholar
  43. Priyanka B, Sekhar K, Reddy VD, Rao KV (2010) Expression of pigeonpea hybrid-proline rice protein encoding gene (CcHyPRP) in yeast and Arabidopsis affords multiple abiotic stress tolerance. Plant Biotechnol J 8:76–87CrossRefPubMedGoogle Scholar
  44. Qian Q, Huang L, Yi R, Wang S, Ding Y (2014) Enhanced resistance to blast fungus in rice (Oryza sativa L.) by expressing the ribosome-inactivating protein α-momorcharin. Plant Sci 217–218:1–7CrossRefPubMedGoogle Scholar
  45. Qiu D, Xiao J, Xie W, Cheng H, Li X, Wang S (2009) Exploring transcriptional signaling mediated by OsWRKY13, a potential regulator of multiple physiological processes in rice. BMC Plant Biol 9:74CrossRefPubMedPubMedCentralGoogle Scholar
  46. Rakwal R, Agrawal GK, Yonekura M (1999) Separation of proteins from stressed rice (Oryza sativa L.) leaf tissues by two-dimensional polyacrylamide gel electrophoresis: induction of pathogenesis-related and cellular protection proteins by jasmonic acid, UV irradiation and copper chloride. Electrophoresis 20:3472–3478CrossRefPubMedGoogle Scholar
  47. Seo Y-S, Chern M, Bartley LE, Han M, Jung K-H, Lee I, Walia H, Richter T, Xu X, Cao P, Bai W, Ramanan R, Amonpant F, Arul L, Canlas PE, Ruan R, Park C-J, Chen X, Hwang S, Jeon J-S, Ronald PC (2011) Towards establishment of a rice stress response interactome. PLoS Genet. CrossRefPubMedPubMedCentralGoogle Scholar
  48. Shaik R, Ramakrishna W (2014) Machine learning approaches distinguish multiple stress conditions using stress-responsive genes and identify candidate genes for broad resistance in rice. Plant Physiol 164:481–495CrossRefPubMedGoogle Scholar
  49. Shao H, Wang H, Tang X (2015) NAC transcription factors in plant multiple abiotic stress responses: progress and prospects. Front Plant Sci. CrossRefPubMedPubMedCentralGoogle Scholar
  50. Sharma R, De Vleesschauwer D, Sharma MK, Ronald PC (2013) Recent advances in dissecting stress-regulatory crosstalk in rice. Mol Plant 6:250–260CrossRefPubMedGoogle Scholar
  51. Shen H, Liu C, Zhang Y, Meng X, Zhou X, Chu C, Wang X (2012) OsWRKY30 is activated by MAP kinases to confer drought tolerance in rice. Plant Mol Biol 80:241–253CrossRefPubMedGoogle Scholar
  52. Singh MP, Lee FN, Counce PA, Gibbons JH (2004) Mediation of partial resistance to rice blast through anaerobic induction of ethylene. Phytopathology 94:819–825CrossRefPubMedGoogle Scholar
  53. Singh P, Sweta K, Mohanapriya A, Sudandiradoss C, Siva R, Gothandam KM, Babu S (2015) Homotypic clustering of OsMYB4 binding site motifs in promoters of the rice genome and cellular-level implications on sheath blight disease resistance. Gene 561:209–218CrossRefGoogle Scholar
  54. Sun L, Huang L, Hong Y, Zhang H, Song F, Li D (2015) Comprehensive analysis suggests overlapping expression of rice ONAC transcription factors in abiotic and biotic stress responses. Int J Mol Sci 16:4306–4326CrossRefPubMedPubMedCentralGoogle Scholar
  55. Tao Z, Kou Y, Liu H, Li X, Xiao J, Wang S (2011) OsWRKY45 alleles play different roles in abscisic acid signaling and salt stress tolerance but similar roles in drought and cold tolerance in rice. J Exp Bot 62:4863–4874CrossRefPubMedPubMedCentralGoogle Scholar
  56. Ueno Y, Yoshida R, Kishi-Kaboshi M, Matsushita A, Jiang C-J, Goto S, Takashashi A, Hirochika H, Takatsuji H (2015) Abiotic stress antagonize the rice defence pathway through the tyrosine-dephosphorylation of OsMPK6. PLoS Pathog 11:e1005231. CrossRefPubMedPubMedCentralGoogle Scholar
  57. van Eck L, Davidson RM, Wu S, Zhao BY, Botha AM, Leach JE, Lapitan NL (2014) The transcriptional network of WRKY53 in cereals links oxidative responses to biotic and abiotic stress inputs. Funct Integr Genom 14:351–362CrossRefGoogle Scholar
  58. Vidhyasekaran P (2007) Fungal pathogenesis in plants and crops: molecular biology and host defense mechanisms. CRC Press, Boca Raton, p 536CrossRefGoogle Scholar
  59. Vogt T (2010) Phenylpropanoid biosynthesis. Mol Plant 3:2–20CrossRefPubMedGoogle Scholar
  60. Wang F, Wang C, Liu P, Lei C, Hao W, Gao Y, Liu YG, Zhao K (2016) Enhanced rice blast resistance by CRISPR/Cas9-targeted mutagenesis of the ERF transcription factor gene OsERF922. PLoS One 11:e0154027CrossRefPubMedPubMedCentralGoogle Scholar
  61. Xiao J, Cheng H, Li X, Xiao J, Xu C, Wang S (2013) Rice WRKY13 regulates cross talk between abiotic and biotic stress signaling pathways by selecting binding to different cis-elements. Plant Physiol 163:1868–1882CrossRefPubMedPubMedCentralGoogle Scholar
  62. Yang DL, Yang Y, He Z (2013) Role of plant hormones and their interplay in rice immunity. Mol Plant 6:675–685CrossRefPubMedGoogle Scholar
  63. Yoo SD, Cho Y, Sheen J (2009) Emerging connections in the ethylene signaling network. Trends Plant Sci 14:270–279CrossRefPubMedPubMedCentralGoogle Scholar
  64. Yun C-S, Motoyama T, Osada H (2015) Biosynthesis of the mycotoxin tenuazonic acid by a fungal NRPS–PKS hybrid enzyme. Nat Commun. CrossRefPubMedPubMedCentralGoogle Scholar
  65. Zhang H, Zhang X, Mao B, Li Q, He Z (2004) Alpha-picolinic acid, a fungal toxin and mammal apoptosis-inducing agent, elicits hypersensitive-like response and enhances disease resistance in rice. Cell Res 14:27–33CrossRefPubMedGoogle Scholar
  66. Zhang YP, ZG E, Jiang H, Wang L, Zhou J, Zhu DF (2015) A comparative study of stress-related gene expression under single stress and intercross stress in rice. Genet Mol Res 14:3702–3717CrossRefPubMedGoogle Scholar
  67. Zhu F, Zhang P, Meng YF, Xu F, Zhang DW, Cheng J, Lin HH, Xi DH (2013) Alpha-momorcharin, a RIP produced by bitter melon, enhances defense response in tobacco plants against diverse plant viruses and shows antifungal activity in vitro. Planta 237:77–88CrossRefPubMedGoogle Scholar

Copyright information

© Franciszek Górski Institute of Plant Physiology, Polish Academy of Sciences, Kraków 2018

Authors and Affiliations

  1. 1.School of Bio Sciences and TechnologyVIT UniversityVelloreIndia

Personalised recommendations