Advertisement

Molecular Biotechnology

, Volume 60, Issue 8, pp 636–650 | Cite as

Combinatorial Interactions of Biotic and Abiotic Stresses in Plants and Their Molecular Mechanisms: Systems Biology Approach

  • Arun Kumar Dangi
  • Babita Sharma
  • Ishu Khangwal
  • Pratyoosh Shukla
Review

Abstract

Plants are continually facing biotic and abiotic stresses, and hence, they need to respond and adapt to survive. Plant response during multiple and combined biotic and abiotic stresses is highly complex and varied than the individual stress. These stresses resulted alteration of plant behavior through regulating the levels of microRNA, heat shock proteins, epigenetic variations. These variations can cause many adverse effects on the growth and development of the plant. Further, in natural conditions, several abiotic stresses causing factors make the plant more susceptible to pathogens infections and vice-versa. A very intricate and multifaceted interactions of various biomolecules are involved in metabolic pathways that can direct towards a cross-tolerance and improvement of plant’s defence system. Systems biology approach plays a significant role in the investigation of these molecular interactions. The valuable information obtained by systems biology will help to develop stress-resistant plant varieties against multiple stresses. Thus, this review aims to decipher various multilevel interactions at the molecular level under combinatorial biotic and abiotic stresses and the role of systems biology to understand these molecular interactions.

Keywords

Plant stress Systems biology MicroRNA Heat shock proteins Biotic and abiotic stresses Molecular mechanisms Stress priming 

Notes

Acknowledgements

The authors acknowledge Maharshi Dayanand University, Rohtak, India for providing infrastructure and lab facility. PS acknowledges the infrastructural support from Department of Science and Technology, Govt. of India through FIST grant (Grant No. 1196 SR/FST/LS-I/2017/4).

Compliance with Ethical Standards

Conflict of interest

All authors declare that they have no conflict of interest.

References

  1. 1.
    Foyer, C. H., Rasool, B., Davey, J. W., & Hancock, R. D. (2016). Cross-tolerance to biotic and abiotic stresses in plants: A focus on resistance to aphid infestation. Journal of Experimental Botany, 67, 2025–2037.CrossRefPubMedGoogle Scholar
  2. 2.
    Calanca, P. P. (2017) Effects of abiotic stress in crop production. In M. Ahmed (Eds.), Quantification of climate variability, adaptation and mitigation for agricultural sustainability (pp. 165–180). New York: Springer.CrossRefGoogle Scholar
  3. 3.
    Nath, M., Bhatt, D., Prasad, R., & Tuteja, N. (2017) Reactive oxygen species (ros) metabolism and signaling in plant-mycorrhizal association under biotic and abiotic stress conditions. In Mycorrhiza-eco-physiology, secondary metabolites, nanomaterials (pp. 223–232). New York: Springer.CrossRefGoogle Scholar
  4. 4.
    Klanderud, K., Meineri, E., Töpper, J., Michel, P., & Vandvik, V. (2017). Biotic interaction effects on seedling recruitment along bioclimatic gradients: Testing the stress-gradient hypothesis. Journal of Vegetation Science, 28, 347–356.CrossRefGoogle Scholar
  5. 5.
    Imam, J., Alam, S., Mandal, N. P., Shukla, P., Sharma, T. R., & Variar, M. (2015). Molecular identification and virulence analysis of AVR genes in rice blast pathogen, Magnaporthe oryzae from Eastern India. Euphytica, 206, 21–31.CrossRefGoogle Scholar
  6. 6.
    Gupta, A., & Senthil-Kumar, M. (2017). Concurrent stresses are perceived as new state of stress by the plants: Overview of impact of abiotic and biotic stress combinations. In M. Senthil-Kumar (Ed.), Plant tolerance to individual and concurrent stresses (pp. 1–15). New Delhi: Springer.Google Scholar
  7. 7.
    Muthusamy, S. K., Dalal, M., Chinnusamy, V., & Bansal, K. C. (2017). Genome-wide identification and analysis of biotic and abiotic stress regulation of small heat shock protein (HSP20) family genes in bread wheat. Journal of Plant Physiology, 211, 100–113.CrossRefPubMedGoogle Scholar
  8. 8.
    Murcia, G., Fontana, A., Pontin, M., Baraldi, R., Bertazza, G., & Piccoli, P. N. (2017). ABA and GA 3 regulate the synthesis of primary and secondary metabolites related to alleviation from biotic and abiotic stresses in grapevine. Phytochemistry, 135, 34–52.CrossRefPubMedGoogle Scholar
  9. 9.
    Bagati, S., Mahajan, R., Nazir, M., Dar, A. A., & Zargar, S. M. (2018). “Omics”: A gateway towards abiotic stress tolerance. In S. Zargar, M. Zargar (Eds.), Abiotic stress-mediated sensing and signaling in plants: An omics perspective (pp. 1–45). Singapore: Springer.Google Scholar
  10. 10.
    Giarola, V., Hou, Q., & Bartels, D. (2017). Angiosperm plant desiccation tolerance: Hints from transcriptomics and genome sequencing. Trends in Plant Science, 22, 705–717.CrossRefPubMedGoogle Scholar
  11. 11.
    Kumar, V., Baweja, M., Singh, P. K., & Shukla, P. (2016). Recent developments in systems biology and metabolic engineering of plant-microbe interactions. Frontiers in Plant Science, 7, 1–12.Google Scholar
  12. 12.
    Imam, J., Mandal, N. P., Variar, M., & Shukla, P. (2016). Advances in molecular mechanism toward understanding plant-microbe interaction: A study of M. oryzae versus rice. In P. Shukla (Ed.), Frontier discoveries and innovations in interdisciplinary microbiology (pp. 79–96). New Delhi: Springer.CrossRefGoogle Scholar
  13. 13.
    Zhai, N., Jia, H., Liu, D., Liu, S., Ma, M., Guo, X., et al. (2017). GhMAP3K65, a cotton Raf-like MAP3K gene, enhances susceptibility to pathogen infection and heat stress by negatively modulating growth and development in transgenic Nicotiana benthamiana. International Journal of Molecular Sciences, 18, 2462.CrossRefPubMedCentralGoogle Scholar
  14. 14.
    Reiss, A., & Jørgensen, L. N. (2017). Biological control of yellow rust of wheat (Puccinia striiformis) with Serenade® ASO (Bacillus subtilis strain QST713). Crop Protection, 93, 1–8.CrossRefGoogle Scholar
  15. 15.
    Vandereyken, K., Hulsmans, S., Broeckx, T., Van Leene, J., Rolland, F., & De Jaeger, G. (2017) The Arabidopsis thaliana LSU peptides: Using an interactomics-based approach to unravel their role in the plant stress response.VIB Conference.Google Scholar
  16. 16.
    Garcia-Molina, A., Altmann, M., Alkofer, A., Epple, P. M., Dangl, J. L., & Falter-Braun, P. (2017). LSU network hubs integrate abiotic and biotic stress responses via interaction with the superoxide dismutase FSD2. Journal of Experimental Botany, 68, 1185–1197.CrossRefPubMedPubMedCentralGoogle Scholar
  17. 17.
    Ramegowda, V., Senthil-Kumar, M., Ishiga, Y., Kaundal, A., Udayakumar, M., & Mysore, K. S. (2013). Drought stress acclimation imparts tolerance to Sclerotinia sclerotiorum and Pseudomonas syringae in Nicotiana benthamiana. International Journal of Molecular Sciences, 14(5), 9497–9513.CrossRefPubMedPubMedCentralGoogle Scholar
  18. 18.
    Rejeb, I. B., Pastor, V., & Mauch-Mani, B. (2014). Plant responses to simultaneous biotic and abiotic stress: Molecular mechanisms. Plants, 3, 458–475.CrossRefPubMedPubMedCentralGoogle Scholar
  19. 19.
    Kariola, T., Brader, G., Helenius, E., Li, J., Heino, P., & Palva, E. T. (2006). Early responsive to dehydration 15, a negative regulator of abscisic acid responses in Arabidopsis. Plant Physiology, 142(4), 1559–1573.CrossRefPubMedPubMedCentralGoogle Scholar
  20. 20.
    Lim, C. W., Baek, W., Jung, J., Kim, J. H., & Lee, S. C. (2015). Function of ABA in stomatal defense against biotic and drought stresses. International Journal of Molecular Sciences, 16, 15251–15270.CrossRefPubMedPubMedCentralGoogle Scholar
  21. 21.
    Lee, S. C., & Luan, S. (2012). ABA signal transduction at the crossroad of biotic and abiotic stress responses. Plant Cell Environment, 35(1), 53–60.CrossRefGoogle Scholar
  22. 22.
    Forcat, S., Bennett, M. H., Mansfield, J. W., & Grant, M. R. (2008). A rapid and robust method for simultaneously measuring changes in the phytohormones ABA, JA and SA in plants following biotic and abiotic stress. Plant Methods, 4(1), 16.CrossRefPubMedPubMedCentralGoogle Scholar
  23. 23.
    Choudhary, K. M. K. A., Chaudhary, N., & Agrawal, S. B. (2017) Reactive oxygen species: Generation, damage, and quenching in plants during stress. In Revisiting role reactive oxygen species plants ROS boon or bane plants? (p. 89). Hoboken: WileyCrossRefGoogle Scholar
  24. 24.
    Jiang, J., Ma, S., Ye, N., Jiang, M., Cao, J., & Zhang, J. (2017). WRKY transcription factors in plant responses to stresses. Journal of Integrative Plant Biology, 59, 86–101.CrossRefPubMedGoogle Scholar
  25. 25.
    López-Galiano, M. J., González-Hernández, A. I., Crespo-Salvador, O., Rausell, C., Real, M. D., Escamilla, M., et al. (2017) Epigenetic regulation of the expression of WRKY75 transcription factor in response to biotic and abiotic stresses in Solanaceae plants. Plant Cell Reports, 37, 1–10.Google Scholar
  26. 26.
    Piya, S., Shrestha, S. K., Binder, B., Stewart, C. N. Jr., & Hewezi, T. (2014). Protein-protein interaction and gene co-expression maps of ARFs and Aux/IAAs in Arabidopsis. Frontiers in Plant Science, 5, 744.CrossRefPubMedPubMedCentralGoogle Scholar
  27. 27.
    Dang, F., Wang, Y., She, J., Lei, Y., Liu, Z., Eulgem, T., Guan, D., et al. (2014). Overexpression of CaWRKY27, a subgroup IIe WRKY transcription factor of Capsicum annuum, positively regulates tobacco resistance to Ralstonia solanacearum infection. Physiologia Plantarum, 150(3), 397–411.CrossRefPubMedGoogle Scholar
  28. 28.
    Li, J., Wang, J., Wang, N., Guo, X., & Gao, Z. (2015). GhWRKY44, a WRKY transcription factor of cotton, mediates defense responses to pathogen infection in transgenic Nicotiana benthamiana. Plant Cell Tissue Organ Culture (PCTOC), 121, 127–140.CrossRefGoogle Scholar
  29. 29.
    Wang, J., Tao, F., An, F., Zou, Y., Tian, W., Chen, X., et al. (2017). Wheat transcription factor TaWRKY70 is positively involved in high-temperature seedling plant resistance to Puccinia striiformis f. sp. tritici. Molecular Plant Pathology, 18, 649–661.CrossRefPubMedGoogle Scholar
  30. 30.
    Liu, X., Song, Y., Xing, F., Wang, N., Wen, F., & Zhu, C. (2016). GhWRKY25, a group I WRKY gene from cotton, confers differential tolerance to abiotic and biotic stresses in transgenic Nicotiana benthamiana. Protoplasma, 253, 1265–1281.CrossRefPubMedGoogle Scholar
  31. 31.
    Cai, H., Yang, S., Yan, Y., Xiao, Z., Cheng, J., Wu, J., Huang, R., et al. (2015). CaWRKY6 transcriptionally activates CaWRKY40, regulates Ralstonia solanacearum resistance, and confers high-temperature and high-humidity tolerance in pepper. Journal of Experimental Botany, 66(11), 3163–3174.CrossRefPubMedGoogle Scholar
  32. 32.
    Wang, G., Zhang, S., Ma, X., Wang, Y., Kong, F., & Meng, Q. (2016). A stress-associated NAC transcription factor (SlNAC35) from tomato plays a positive role in biotic and abiotic stresses. Physiologia Plantarum, 158, 45–64.CrossRefPubMedGoogle Scholar
  33. 33.
    McGrann, G. R., Steed, A., Burt, C., Goddard, R., Lachaux, C., Bansal, A., et al. (2015). Contribution of the drought tolerance-related stress-responsive NAC1 transcription factor to resistance of barley to Ramularia leaf spot. ‎Mol. Plant Pathology, 16, 201–209.Google Scholar
  34. 34.
    Amorim, A., Lidiane, L. B., da Fonseca dos Santos, R., Pacifico Bezerra Neto, J., Guida-Santos, M., Crovella, S., et al. (2017). Transcription factors involved in plant resistance to pathogens. Current Protein and Peptide Science, 18, 335–351.CrossRefPubMedGoogle Scholar
  35. 35.
    Tak, H., Negi, S., & Ganapathi, T. R. (2017). Banana NAC transcription factor MusaNAC042 is positively associated with drought and salinity tolerance. Protoplasma, 254, 803–816.CrossRefPubMedGoogle Scholar
  36. 36.
    Qin, Y., Tian, Y., & Liu, X. (2015) A wheat salinity-induced WRKY transcription factor TaWRKY93 confers multiple abiotic stress tolerance in Arabidopsis thaliana. ‎Biochemical Biophysical Research Communication 464, 428–433.CrossRefGoogle Scholar
  37. 37.
    Wang, G., Zhang, S., Ma, X., Wang, Y., Kong, F., & Meng, Q. (2016). A stress-associated NAC transcription factor (SlNAC35) from tomato plays a positive role in biotic and abiotic stresses. Physiologia Plantarum, 158(1), 45–64.CrossRefPubMedGoogle Scholar
  38. 38.
    Nakashima, K., Tran, L. S. P., Van Nguyen, D., Fujita, M., Maruyama, K., Todaka, D., Yamaguchi-Shinozaki, K., et al. (2007). Functional analysis of a NAC-type transcription factor OsNAC6 involved in abiotic and biotic stress-responsive gene expression in rice. The Plant Journal, 51(4), 617–630.CrossRefPubMedGoogle Scholar
  39. 39.
    Xie, F., Frazier, T. P., & Zhang, B. (2010). Identification and characterization of microRNAs and their targets in the bioenergy plant switchgrass (Panicum virgatum). Planta, 232(2), 417–434.CrossRefPubMedGoogle Scholar
  40. 40.
    Li, H., Wang, Y., Wu, M., Li, L., Li, C., Han, Z., et al. (2017). Genome-wide identification of AP2/ERF transcription factors in cauliflower and expression profiling of the ERF family under salt and drought stresses. Frontier Plant Science, 8, 946.CrossRefGoogle Scholar
  41. 41.
    Wuddineh, W. A., Mazarei, M., Turner, G. B., Sykes, R. W., Decker, S. R., Davis, M. F., & Stewart, C. N. Jr. (2015). Identification and molecular characterization of the switchgrass AP2/ERF transcription factor superfamily, and overexpression of PvERF001 for improvement of biomass characteristics for biofuel. Frontiers in Bioengineering and Biotechnology, 3, 101.CrossRefPubMedPubMedCentralGoogle Scholar
  42. 42.
    Mishra, S., Phukan, U. J., Tripathi, V., Singh, D. K., Luqman, S., & Shukla, R. K. (2015). PsAP2 an AP2/ERF family transcription factor from Papaver somniferum enhances abiotic and biotic stress tolerance in transgenic tobacco. Plant Molecular Biology, 89(1–2), 173–186.CrossRefPubMedGoogle Scholar
  43. 43.
    Phukan, U. J., Jeena, G. S., & Shukla, R. K. (2016). WRKY transcription factors: Molecular regulation and stress responses in plants. Frontiers in Plant Science, 7, 760.CrossRefPubMedPubMedCentralGoogle Scholar
  44. 44.
    Parveda, M., Kiran, B., Punita, D. L., & Kishor, P. B. K. (2017). Overexpression of SbAP37 in rice alleviates concurrent imposition of combination stresses and modulates different sets of leaf protein profiles. Plant Cell Reports, 36, 773–786.CrossRefPubMedGoogle Scholar
  45. 45.
    Jisha, V., Dampanaboina, L., Vadassery, J., Mithöfer, A., Kappara, S., & Ramanan, R. (2015). Overexpression of an AP2/ERF type transcription factor OsEREBP1 confers biotic and abiotic stress tolerance in rice. PLoS ONE, 10, 0127831.CrossRefGoogle Scholar
  46. 46.
    Chen, X., & Guo, Z. (2008). Tobacco OPBP1 enhances salt tolerance and disease resistance of transgenic rice. International Journal of Molecular Sciences, 9(12), 2601–2613.CrossRefPubMedPubMedCentralGoogle Scholar
  47. 47.
    Tardif, G., Kane, N. A., Adam, H., Labrie, L., Major, G., Gulick, P., et al. (2007). Interaction network of proteins associated with abiotic stress response and development in wheat. Plant Molecular Biology, 63, 703–718.CrossRefPubMedGoogle Scholar
  48. 48.
    Qi, Z., Yu, J., Shen, L., Yu, Z., Yu, M., Du, Y., et al. (2017). Enhanced resistance to rice blast and sheath blight in rice (Oryza sativa L.) by expressing the oxalate decarboxylase protein Bacisubin from Bacillus subtilis. Plant Science, 265, 51–60.CrossRefPubMedGoogle Scholar
  49. 49.
    Choudhury, F. K., Rivero, R. M., Blumwald, E., & Mittler, R. (2017). Reactive oxygen species, abiotic stress and stress combination. The Plant Journal, 90, 856–867.CrossRefPubMedGoogle Scholar
  50. 50.
    Dar, M. I., Naikoo, M. I., Khan, F. A., Rehman, F., Green, I. D., Naushin, F., et al. (2017). An introduction to reactive oxygen species metabolism under changing climate in plants. In M. I. R. Khan, N. A. Khan (Eds.), Reactive oxygen species and antioxidant systems in plants: Role and regulation under abiotic stress (pp. 25–52). Singapore: Springer.CrossRefGoogle Scholar
  51. 51.
    Raja, V., Majeed, U., Kang, H., Andrabi, K. I., & John, R. (2017). Abiotic stress: Interplay between ROS, hormones and MAPKs. Environmental and Experimental Botany, 137, 142–157.CrossRefGoogle Scholar
  52. 52.
    Dauphinee, A. N., Fletcher, J. I., Denbigh, G. L., Lacroix, C. R., & Gunawardena, A. H. (2017) Remodelling of lace plant leaves: Antioxidants and ROS are key regulators of programmed cell death. Planta, 246, 1–15.CrossRefGoogle Scholar
  53. 53.
    Van Aken, O., & Pogson, B. J. (2017). Convergence of mitochondrial and chloroplastic ANAC017/PAP-dependent retrograde signalling pathways and suppression of programmed cell death. Cell Death and Differentiation, 24, 955–960.CrossRefPubMedPubMedCentralGoogle Scholar
  54. 54.
    Mittler, R. (2017). ROS are good. Trends in Plant Science, 22, 11–19.CrossRefPubMedGoogle Scholar
  55. 55.
    Willems, P., Mhamdi, A., Simon, S., Storme, V., Kerchev, P. I., Noctor, G., et al. (2016) The ROS wheel: Refining ROS transcriptional footprints in Arabidopsis. Plant Physiology.  https://doi.org/10.1104/pp.16.00420.CrossRefPubMedPubMedCentralGoogle Scholar
  56. 56.
    Jalmi, S. K., & Sinha, A. K. (2015) ROS mediated MAPK signaling in abiotic and biotic stress-striking similarities and differences. Frontiers Plant Science 6, 769CrossRefGoogle Scholar
  57. 57.
    Hu, Y., You, J., Li, C., Hua, C., & Wang, C. (2017). Exogenous application of methyl jasmonate induces defence against Meloidogyne hapla in soybean. Nematology, 19, 293–304.CrossRefGoogle Scholar
  58. 58.
    Davletova, S., Schlauch, K., Coutu, J., & Mittler, R. (2005). The zinc-finger protein Zat12 plays a central role in reactive oxygen and abiotic stress signaling in Arabidopsis. Plant Physiology, 139(2), 847–856.CrossRefPubMedPubMedCentralGoogle Scholar
  59. 59.
    Laluk, K., AbuQamar, S., & Mengiste, T. (2011). The Arabidopsis mitochondria-localized pentatricopeptide repeat protein PGN functions in defense against necrotrophic fungi and abiotic stress tolerance. Plant Physiology, 156(4), 2053–2068.CrossRefPubMedPubMedCentralGoogle Scholar
  60. 60.
    Chardin, C., Schenk, S. T., Hirt, H., Colcombet, J., & Krapp, A. (2017). Mitogen-activated protein kinases in nutritional signaling in Arabidopsis. Plant Science, 260, 101–108.CrossRefPubMedGoogle Scholar
  61. 61.
    de Zelicourt, A., Colcombet, J., & Hirt, H. (2016). The role of MAPK modules and ABA during abiotic stress signaling. Trends Plant Science, 21(8), 677–685.CrossRefGoogle Scholar
  62. 62.
    Ning, J., Li, X., Hicks, L. M., & Xiong, L. (2010). A Raf-like MAPKKK gene DSM1 mediates drought resistance through reactive oxygen species scavenging in rice. Plant Physiology, 152, 876–890.CrossRefPubMedPubMedCentralGoogle Scholar
  63. 63.
    Berriri, S., Garcia, A. V., ditFrey, N. F., Rozhon, W., Pateyron, S., Leonhardt, N., et al. (2012). Constitutively active mitogen-activated protein kinase versions reveal functions of Arabidopsis MPK4 in pathogen defense signaling. The Plant Cell, 24, 4281–4293.CrossRefPubMedPubMedCentralGoogle Scholar
  64. 64.
    Kimura, S., Waszczak, C., Hunter, K., & Wrzaczek, M. (2017). Bound by fate: The role of reactive oxygen species in receptor-like kinase signaling. The Plant Cell, 29, 638–654.CrossRefPubMedPubMedCentralGoogle Scholar
  65. 65.
    Furuya, T., Matsuoka, D., & Nanmori, T. (2014). Membrane rigidification functions upstream of the MEKK1-MKK2-MPK4 cascade during cold acclimation in Arabidopsis thaliana. FEBS Letters, 588(11), 2025–2030.CrossRefPubMedGoogle Scholar
  66. 66.
    Benhamman, R., Bai, F., Drory, S. B., Loubert-Hudon, A., Ellis, B., & Matton, D. P. (2017). The Arabidopsis mitogen-activated protein kinase kinase kinase 20 (MKKK20) acts upstream of MKK3 and MPK18 in two separate signaling pathways involved in root microtubule functions. Frontiers in Plant Science, 8, 1352.CrossRefPubMedPubMedCentralGoogle Scholar
  67. 67.
    Sharma, R., De Vleesschauwer, D., Sharma, M. K., & Ronald, P. C. (2013). Recent advances in dissecting stress-regulatory crosstalk in rice. Molecular Plant, 6(2), 250–260.CrossRefPubMedGoogle Scholar
  68. 68.
    Jacob, P., Hirt, H., & Bendahmane, A. (2017). The heat-shock protein/chaperone network and multiple stress resistance. Plant Biotechnology Journal, 15, 405–414.CrossRefPubMedPubMedCentralGoogle Scholar
  69. 69.
    Haak, D. C., Fukao, T., Grene, R., Hua, Z., Ivanov, R., Perrella, G., et al. (2017). Multilevel regulation of abiotic stress responses in plants. Frontiers in Plant Science, 8, 1564.CrossRefPubMedPubMedCentralGoogle Scholar
  70. 70.
    Nejat, N., & Mantri, N. (2017). Plant immune system: Crosstalk between responses to biotic and abiotic stresses the missing link in understanding plant defence. Current Issues in Molecular Biology, 23, 1–16.CrossRefPubMedGoogle Scholar
  71. 71.
    Lopes-Caitar, V. S., Silva, S. M. H., & Marcelino-Guimaraes, F. C. (2016) Plant small heat shock proteins and its interactions with biotic stress. In A. Asea, P. Kaur, & S. Calderwood (Eds.), Heat shock proteins and plants (Vol. 10, pp. 19–39). Cham: SpringerCrossRefGoogle Scholar
  72. 72.
    Cheng, Z.-W., Chen, Z.-Y., Yan, X., Bian, Y.-W., Deng, X., & Yan, Y.-M. (2018). Integrated physiological and proteomic analysis reveals underlying response and defense mechanisms of Brachypodium distachyon seedling leaves under osmotic stress, cadmium and their combined stresses. Journal of Proteomics, 170, 1–13.CrossRefPubMedGoogle Scholar
  73. 73.
    Wu, Y., Yang, L., Yu, M., & Wang, J. (2017). Identification and expression analysis of microRNAs during ovule development in rice (Oryza sativa) by deep sequencing. Plant Cell Reports, 36, 1815–1827.CrossRefPubMedGoogle Scholar
  74. 74.
    Chinnusamy, V., Zhu, J., & Zhu, J.-K. (2007). Cold stress regulation of gene expression in plants. Trends in Plant Science, 12, 444–451.CrossRefPubMedGoogle Scholar
  75. 75.
    Shriram, V., Kumar, V., Devarumath, R. M., Khare, T. S., & Wani, S. H. (2016). MicroRNAs as potential targets for abiotic stress tolerance in plants. Frontiers in Plant Science 7, 1–18.CrossRefGoogle Scholar
  76. 76.
    Taxak, P. C., Khanna, S. M., Bharadwaj, C., Gaikwad, K., Kaur, S., Chopra, M., Kumar, D., et al. (2017). Transcriptomic signature of Fusarium toxin in chickpea unveiling wilt pathogenicity pathways and marker discovery. Physiological Molecular Plant Pathology, 100, 163–177.CrossRefGoogle Scholar
  77. 77.
    Nasir, F., Tian, L., Chang, C., Li, X., Gao, Y., Tran, L. S. P., & Tian, C. (2017) Current understanding of pattern-triggered immunity and hormone-mediated defense in rice (Oryza sativa) in response to Magnaporthe oryzae infection. In Seminars in cell & developmental biology. Cambridge: Academic Press.Google Scholar
  78. 78.
    Jagadeeswaran, G., Saini, A., & Sunkar, R. (2009). Biotic and abiotic stress down-regulate miR398 expression in Arabidopsis. Planta., 229(4), 1009–1014.CrossRefPubMedGoogle Scholar
  79. 79.
    Kulcheski, F. R., de Oliveira, L. F., Molina, L. G., Almerão, M. P., Rodrigues, F. A., Marcolino, J., Abdelnoor, R. V., et al. (2011). Identification of novel soybean microRNAs involved in abiotic and biotic stresses. BMC Genomics, 12(1), 307.CrossRefPubMedPubMedCentralGoogle Scholar
  80. 80.
    Sanan-Mishra, N., Kumar, V., Sopory, S. K., & Mukherjee, S. K. (2009). Cloning and validation of novel miRNA from basmati rice indicates cross talk between abiotic and biotic stresses. Molecular Genetics Genomics, 282(5), 463.CrossRefPubMedGoogle Scholar
  81. 81.
    Xin, M., Wang, Y., Yao, Y., Song, N., Hu, Z., Qin, D., Sun, Q., et al. (2011). Identification and characterization of wheat long non-protein coding RNAs responsive to powdery mildew infection and heat stress by using microarray analysis and SBS sequencing. BMC Plant Biology, 11(1), 61.CrossRefPubMedPubMedCentralGoogle Scholar
  82. 82.
    Zhao, J. P., Jiang, X. L., Zhang, B. Y., & Su, X. H. (2012) Involvement of microRNA-mediated gene expression regulation in the pathological development of stem canker disease in Populus trichocarpa. PLoS ONE, 7(9), e44968.CrossRefPubMedPubMedCentralGoogle Scholar
  83. 83.
    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 Biology, 10, 56.CrossRefPubMedPubMedCentralGoogle Scholar
  84. 84.
    Fortes, A. M., & Gallusci, P. (2017). Plant stress responses and phenotypic plasticity in the epigenomics era: Perspectives on the grapevine scenario, a model for perennial crop plants. Frontiers in Plant Science, 8, 82PubMedPubMedCentralGoogle Scholar
  85. 85.
    Gallusci, P., Dai, Z., Génard, M., Gauffretau, A., Leblanc-Fournier, N., Richard-Molard, C., et al. (2017). Epigenetics for plant improvement: Current knowledge and modeling avenues. Trends in Plant Science, 22, 610–623.CrossRefPubMedGoogle Scholar
  86. 86.
    Seymour, D. K., & Becker, C. (2017). The causes and consequences of DNA methylome variation in plants. Current Opinion in Plant Biology, 36, 56–63.CrossRefPubMedGoogle Scholar
  87. 87.
    Lämke, J., & Bäurle, I. (2017). Epigenetic and chromatin-based mechanisms in environmental stress adaptation and stress memory in plants. Genome Biology, 18, 124.CrossRefPubMedPubMedCentralGoogle Scholar
  88. 88.
    Srivastava, A. K., Lu, Y., Zinta, G., Lang, Z., & Zhu, J.-K. (2017). UTR-dependent control of gene expression in plants. Trends Plant Science.  https://doi.org/10.1016/j.tplants.2017.11.003.CrossRefGoogle Scholar
  89. 89.
    Springer, N. M., & Schmitz, R. J. (2017). Exploiting induced and natural epigenetic variation for crop improvement. Nature Reviews Genetics, 18, 563.CrossRefPubMedGoogle Scholar
  90. 90.
    Wang, X., Zhang, Z., Fu, T., Hu, L., Xu, C., Gong, L., et al. (2017) Gene-body CG methylation and divergent expression of duplicate genes in rice. Scientific Reports, 7, 2675CrossRefPubMedPubMedCentralGoogle Scholar
  91. 91.
    Yu, A., Lepère, G., Jay, F., Wang, J., Bapaume, L., Wang, Y., Navarro, L., et al. (2013). Dynamics and biological relevance of DNA demethylation in Arabidopsis antibacterial defense. Proceedings of the National Academy of Sciences, 110(6), 2389–2394.CrossRefGoogle Scholar
  92. 92.
    Singh, A., Ganapathysubramanian, B., Singh, A. K., & Sarkar, S. (2016). Machine learning for high-throughput stress phenotyping in plants. Trends in Plant Science, 21(2), 110–124.CrossRefPubMedGoogle Scholar
  93. 93.
    Hashida, S. N., Takahashi, H., & Uchimiya, H. (2009). The role of NAD biosynthesis in plant development and stress responses. Annals of Botany, 103(6), 819–824.CrossRefPubMedPubMedCentralGoogle Scholar
  94. 94.
    Kumar Singh, P., Shukla, P., Singh, P. K., & Shukla, P. (2015). Systems biology as an approach for deciphering microbial interactions. Briefings in Functional Genomics, 14, 166–168.CrossRefPubMedGoogle Scholar
  95. 95.
    Bhardwaj, T., & Somvanshi, P. (2015). Plant systems biology: Insights and advancements. In D. Barh, M. Khan & E. Davies (Eds.), PlantOmics: The omics of plant science (pp. 791–819). New Delhi: Springer.Google Scholar
  96. 96.
    Dangi, A. K., Dubey, K. K., & Shukla, P. (2017). Strategies to improve Saccharomyces cerevisiae: Technological advancements and evolutionary engineering. Indian Journal of Microbiology, 57, 378–386.CrossRefPubMedGoogle Scholar
  97. 97.
    Imam, J., Mandal, N. P., Variar, M., & Shukla, P. (2016). Advances in molecular mechanism toward understanding plant-microbe interaction: A study of M. oryzae versus rice. In P. Shukla (Ed.), Frontier discoveries and innovations in interdisciplinary (pp. 79–96). New Delhi: Springer.CrossRefGoogle Scholar
  98. 98.
    Groover, A., & Cronk, Q. (2017) Comparative and evolutionary genomics of angiosperm trees. New York: Springer.CrossRefGoogle Scholar
  99. 99.
    Putman, T. E., Lelong, S., Burgstaller-Muehlbacher, S., Waagmeester, A., DIesh, C., Dunn, N., et al. (2017). WikiGenomes: An open web application for community consumption and curation of gene annotation data in Wikidata. Database 2017, bax025.CrossRefPubMedCentralGoogle Scholar
  100. 100.
    Rasmussen, S., Barah, P., Suarez-Rodriguez, M. C., Bressendorff, S., Friis, P., Costantino, P., et al. (2013). Transcriptome responses to combinations of stresses in Arabidopsis. Plant Physiology, 161, 1783–1794.CrossRefPubMedPubMedCentralGoogle Scholar
  101. 101.
    Powell, J. J., Carere, J., Fitzgerald, T. L., Stiller, J., Covarelli, L., Xu, Q., et al. (2016). The Fusarium crown rot pathogen Fusarium pseudograminearum triggers a suite of transcriptional and metabolic changes in bread wheat (Triticum aestivum L.). Annals of Botany, 119, 853–867.PubMedCentralGoogle Scholar
  102. 102.
    Petitot, A.-S., Kyndt, T., Haidar, R., Dereeper, A., Collin, M., de Almeida Engler, J., et al. (2017). Transcriptomic and histological responses of African rice (Oryza glaberrima) to Meloidogyne graminicola provide new insights into root-knot nematode resistance in monocots. Annals of Botany, 119, 885–899.CrossRefPubMedPubMedCentralGoogle Scholar
  103. 103.
    Arbona, V., Manzi, M., Zandalinas, S. I., Vives-Peris, V., Pérez-Clemente, R. M., & Gómez-Cadenas, A. (2017) Physiological, metabolic, and molecular responses of plants to abiotic stress. In M. Z. Abdin (Ed.), Stress signaling in plants: Genomics and proteomics perspective (pp. 1–35). New Delhi: SpringerGoogle Scholar
  104. 104.
    Qureshi, M. I., Qadir, S., & Zolla, L. (2007). Proteomics-based dissection of stress-responsive pathways in plants. Journal of Plant Physiology, 164, 1239–1260.CrossRefPubMedGoogle Scholar
  105. 105.
    Stare, T., Stare, K., Weckwerth, W., Wienkoop, S., & Gruden, K. (2017). Comparison between proteome and transcriptome response in potato (Solanum tuberosum L.) leaves following potato virus y (pvy) infection. Proteomes, 5, 14.CrossRefPubMedCentralGoogle Scholar
  106. 106.
    Padliya, N. D., & Cooper, B. (2006). Mass spectrometry-based proteomics for the detection of plant pathogens. Proteomics, 6, 4069–4075.CrossRefPubMedGoogle Scholar
  107. 107.
    Li, G., Wu, Y., Liu, G., Xiao, X., Wang, P., Gao, T., et al. (2017). Large-scale proteomics combined with transgenic experiments demonstrates an important role of jasmonic acid in potassium deficiency response in wheat and rice. Molecular and Cellular Proteomics, 16, 1889–1905.CrossRefPubMedGoogle Scholar
  108. 108.
    Zandalinas, S. I., Mittler, R., Balfagón, D., Arbona, V., & Gómez-Cadenas, A. (2017) Plant adaptations to the combination of drought and high temperatures. Physiologia Plantarum 162, 2–12Google Scholar
  109. 109.
    Zhang, M., Xu, J., Liu, G., Yao, X., Ren, R., & Yang, X. (2017) Proteomic analysis of responsive root proteins of Fusarium oxysporum-infected watermelon seedlings. Plant and Soil, 422, 169–181Google Scholar
  110. 110.
    Zhang, H.-Y., Lei, G., Zhou, H.-W., He, C., Liao, J.-L., & Huang, Y.-J. (2017) Quantitative iTRAQ-based proteomic analysis of rice grains to assess high night temperature stress. Proteomics.  https://doi.org/10.1002/pmic.201600365 CrossRefPubMedPubMedCentralGoogle Scholar
  111. 111.
    Kumar Singh, P., & Shukla, P. (2015). Systems biology as an approach for deciphering microbial interactions. Briefings in Functional Genomic Proteomics 14, 166–168.CrossRefGoogle Scholar
  112. 112.
    El Rabey, H. A., Al-Malki, A. L., Abulnaja, K. O., & Rohde, W. (2015) Proteome analysis for understanding abiotic stress (salinity and drought) tolerance in date palm (Phoenix dactylifera L.). International Journal of Genomics.  https://doi.org/10.1155/2015/407165.CrossRefPubMedPubMedCentralGoogle Scholar
  113. 113.
    Al-Obaidi, J. R., Rahmad, N., Hanafi, N. M., Halabi, M. F., & Al-Soqeer, A. A. (2017). Comparative proteomic analysis of male and female plants in jojoba (Simmondsia chinensis) leaves revealed changes in proteins involved in photosynthesis, metabolism, energy, and biotic and abiotic stresses. Acta Physiologiae Plantarum, 39, 179.CrossRefGoogle Scholar
  114. 114.
    Mosa, K. A., Ismail, A., & Helmy, M. (2017). Omics and system biology approaches in plant stress research. In K. A. Mosa, A. Ismail & M. Helmy (Eds.), Plant stress tolerance (pp. 21–34). Cham: Springer.CrossRefGoogle Scholar
  115. 115.
    Obata, T., & Fernie, A. R. (2012). The use of metabolomics to dissect plant responses to abiotic stresses. Cellular and Molecular Life Sciences, 69, 3225–3243.CrossRefPubMedPubMedCentralGoogle Scholar
  116. 116.
    Zhao, L., Huang, Y., Hu, J., Zhou, H., Adeleye, A. S., & Keller, A. A. (2016). 1H NMR and GC-MS based metabolomics reveal defense and detoxification mechanism of cucumber plant under nano-Cu stress. Environmental Science and Technology, 50, 2000–2010.CrossRefPubMedGoogle Scholar
  117. 117.
    Kusano, M., Yang, Z., Okazaki, Y., Nakabayashi, R., Fukushima, A., & Saito, K. (2015). Using metabolomic approaches to explore chemical diversity in rice. Molecular Plant, 8, 58–67.CrossRefPubMedGoogle Scholar
  118. 118.
    Rabara, R. C., Tripathi, P., & Rushton, P. J. (2017) Comparative metabolome profile between tobacco and soybean grown under water-stressed conditions. BioMed Research International.  https://doi.org/10.1155/2017/3065251 CrossRefPubMedPubMedCentralGoogle Scholar
  119. 119.
    Moradi, P., Ford-lloyd, B., & Pritchard, J. (2017). Comprehensive list of metabolites measured by DI-FTICR mass spectrometry in thyme plants with contrasting tolerance to drought. Data in Brief, 12, 438–441.CrossRefPubMedPubMedCentralGoogle Scholar
  120. 120.
    Blum, A. (2018). Plant breeding for stress environments. Boca Raton: CRC press.CrossRefGoogle Scholar
  121. 121.
    Bigelow, P. J., Loescher, W., Hancock, J. F., & Grumet, R.(2018). Influence of intergenotypic competition on multigenerational persistence of abiotic stress resistance transgenes in populations of Arabidopsis thaliana. Evolutionary Applications.  https://doi.org/10.1111/eva.12610 CrossRefPubMedPubMedCentralGoogle Scholar
  122. 122.
    Nogueira, M., Enfissi, E. M., Almeida, J., & Fraser, P. D. (2018). Creating plant molecular factories for industrial and nutritional isoprenoid production. Current Opinion in Biotechnology, 49, 80–87.CrossRefPubMedGoogle Scholar
  123. 123.
    Duhan, J. S., Kumar, R., Kumar, N., Kaur, P., & Nehra, K. (2017) Nanotechnology: The new perspective in precision agriculture. Biotechnology Reports, 15, 11–23.CrossRefPubMedPubMedCentralGoogle Scholar
  124. 124.
    Torney, F., Trewyn, B. G., Lin, V. S.-Y., & Wang, K. (2007). Mesoporous silica nanoparticles deliver DNA and chemicals into plants. Nature Nanotechnology, 2, 295–300.CrossRefPubMedGoogle Scholar
  125. 125.
    Liang, S., Kang, Y., Tiraferri, A., Giannelis, E. P., Huang, X., & Elimelech, M. (2013). Highly hydrophilic polyvinylidene fluoride (PVDF) ultrafiltration membranes via post fabrication grafting of surface-tailored silica nanoparticles. ACS Applied Material Interfaces, 5(14), 6694–6703.CrossRefGoogle Scholar
  126. 126.
    Shen, X., Zhou, Y., Duan, L., Li, Z., Eneji, A. E., & Li, J. (2010). Silicon effects on photosynthesis and antioxidant parameters of soybean seedlings under drought and ultraviolet-B radiation. Journal of Plant Physiology, 167, 1248–1252.CrossRefPubMedGoogle Scholar
  127. 127.
    Xu, C. X., Ma, Y. P., & Liu, Y. L. (2015). Effects of silicon (Si) on growth, quality and ionic homeostasis of aloe under salt stress. South African Journal of Botany, 98, 26–36.CrossRefGoogle Scholar
  128. 128.
    Keller, C., Rizwan, M., Davidian, J. C., Pokrovsky, O. S., Bovet, N., Chaurand, P., & Meunier, J. D. (2015). Effect of silicon on wheat seedlings (Triticum turgidum L.) grown in hydroponics and exposed to 0 to 30 µM Cu. Planta, 241, 847–860.CrossRefPubMedGoogle Scholar
  129. 129.
    Ma, J., Cai, H., He, C., Zhang, W., & Wang, L. (2015). A hemicellulose-bound form of silicon inhibits cadmium ion uptake in rice (Oryza sativa) cells. New Phytologist, 206, 1063–1074.CrossRefPubMedGoogle Scholar
  130. 130.
    Imtiaz, M., Rizwan, M. S., Mushtaq, M. A., Ashraf, M., Shahzad, S. M., Yousaf, B., Saeed, D. A., Rizwan, M., Nawaz, M. A., Mehmood, S., & Tu, S. (2016). Silicon occurrence, uptake, transport and mechanisms of heavy metals, minerals and salinity enhanced tolerance in plants with future prospects: A review. Journal of Environmental Management, 183, 521–529.CrossRefPubMedGoogle Scholar
  131. 131.
    Adrees, M., Ali, S., Rizwan, M., Ibrahim, M., Abbas, F., & Farid, M. (2015). The effect of excess copper on growth and physiology of important food crops: A review. Environmental Science and Pollution Research, 22, 8148–8162.CrossRefPubMedGoogle Scholar
  132. 132.
    Massey, F. P., & Hartley, S. E. (2009). Physical defences wear you down: Progressive and irreversible impacts of silica on insect herbivores. Journal of Animal Ecology, 78, 281–291.CrossRefPubMedGoogle Scholar
  133. 133.
    Rahman, A., Wallis, C. M., & Uddin, W. (2015). Silicon-induced systemic defense responses in perennial rye grass against infection by Magnaporthe oryzae. Phytopathology, 105, 748–757.CrossRefPubMedGoogle Scholar
  134. 134.
    Reynolds, O. L., Padula, M. P., Zeng, R., & Gurr, G. M. (2016) Silicon: Potential to promote direct and indirect effects on plant defense against arthropod pests in agriculture. Frontiers in Plant Science 7, 744CrossRefPubMedPubMedCentralGoogle Scholar
  135. 135.
    Moeller, L., & Wang, K. A. N. (2008). Engineering with precision: Tools for the new generation of transgenic crops. BioScience, 58, 391–401.CrossRefGoogle Scholar
  136. 136.
    Sun, T., Zhang, Y. S., Pang, B., Hyun, D. C., Yang, M., & Xia, Y. (2014). Engineered nanoparticles for drug delivery in cancer therapy. Angewandte Chemie International Edition, 53(46), 12320–12364.PubMedGoogle Scholar
  137. 137.
    Sun, X., He, J., Meng, Y., Zhang, L., Zhang, S., Ma, X., Dey, S., Zhao, J., & Lei, Y. (2016). Microwave-assisted ultrafast and facile synthesis of fluorescent carbon nanoparticles from a single precursor: Preparation, characterization and their application for the highly selective detection of explosive picric acid. Journal of Materials Chemistry A, 4(11), 4161–4171.CrossRefGoogle Scholar
  138. 138.
    Tripathi, B. P., Dubey, N. C., Subair, R., Choudhury, S., & Stamm, M. (2016). Enhanced hydrophilic and antifouling polyacrylonitrile membrane with polydopamine modified silica nanoparticles. RSC Advances, 6(6), 4448–4457.CrossRefGoogle Scholar
  139. 139.
    Luyckx, M., Hausman, J., Lutts, S., & Guerriero, G. (2017). Silicon and plants: Current knowledge and technological perspectives. Frontiers in Plant Science, 8(19), 1–8.Google Scholar
  140. 140.
    Safi, H., Saibi, W., Alaoui, M. M., Hmyene, A., Masmoudi, K., Hanin, M., et al. (2015). A wheat lipid transfer protein (TdLTP4) promotes tolerance to abiotic and biotic stress in Arabidopsis thaliana. Plant Physiology and Biochemistry, 89, 64–75.CrossRefPubMedGoogle Scholar
  141. 141.
    Misra, R. C., Kamthan, M., Kumar, S., & Ghosh, S. (2016). A thaumatin-like protein of Ocimum basilicum confers tolerance to fungal pathogen and abiotic stress in transgenic Arabidopsis. Scientific Reports, 6, 25340.CrossRefPubMedPubMedCentralGoogle Scholar
  142. 142.
    Mellacheruvu, S., Tamirisa, S., Vudem, D. R., & Khareedu, V. R. (2016). Pigeonpea hybrid-proline-rich protein (CcHyPRP) confers biotic and abiotic stress tolerance in transgenic rice. Frontiers in Plant Science, 6, 1167.CrossRefPubMedPubMedCentralGoogle Scholar
  143. 143.
    Wu, J., Folta, K. M., Xie, Y., Jiang, W., Lu, J., & Zhang, Y. (2017). Overexpression of Muscadinia rotundifolia CBF2 gene enhances biotic and abiotic stress tolerance in Arabidopsis. Protoplasma, 254, 239–251.CrossRefPubMedGoogle Scholar
  144. 144.
    Jiang, Y., Duan, Y., Yin, J., Ye, S., Zhu, J., Zhang, F., Luo, K., et al. (2014). Genome-wide identification and characterization of the Populus WRKY transcription factor family and analysis of their expression in response to biotic and abiotic stresses. Journal of Experimental Botany, 65(22), 6629–6644.CrossRefPubMedPubMedCentralGoogle Scholar
  145. 145.
    Kissoudis, C., Chowdhury, R., van Heusden, S., van de Wiel, C., Finkers, R., Visser, R. G., van der Linden, G., et al. (2015). Combined biotic and abiotic stress resistance in tomato. Euphytica, 202(2), 317–332.CrossRefGoogle Scholar
  146. 146.
    Pandey, V., Niranjan, A., Atri, N., Chandrashekhar, K., Mishra, M. K., Trivedi, P. K., & Misra, P. (2014). WsSGTL1 gene from Withania somnifera, modulates glycosylation profile, antioxidant system and confers biotic and salt stress tolerance in transgenic tobacco. Planta, 239(6), 1217–1231.CrossRefPubMedGoogle Scholar
  147. 147.
    Johnson, J. M., Reichelt, M., Vadassery, J., Gershenzon, J., & Oelmüller, R. (2014). An Arabidopsis mutant impaired in intracellular calcium elevation is sensitive to biotic and abiotic stress. BMC Plant Biology, 14(1), 162.CrossRefGoogle Scholar
  148. 148.
    Su, Y., Xu, L., Fu, Z., Yang, Y., Guo, J., Wang, S., & Que, Y. (2014). ScChi, encoding an acidic class III chitinase of sugarcane, confers positive responses to biotic and abiotic stresses in sugarcane. International Journal of Molecular Sciences, 15(2), 2738–2760.CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Enzyme Technology and Protein Bioinformatics Laboratory, Department of MicrobiologyMaharshi Dayanand UniversityRohtakIndia

Personalised recommendations