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Leaf wax trait in crops for drought and biotic stress tolerance: regulators of epicuticular wax synthesis and role of small RNAs

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Abstract

Climate-smart agriculture, an approach evolved to develop and guide actions needed to transform agricultural systems in a changing climate is being encouraged globally to ensure food security. Climatic variables termed as abiotic stresses affect crop production and food quality. Amongst various abiotic stresses, drought is the major one, especially in tropical countries, the occurrence of which can alter biotic stress (plant–pest/pathogen) interactions. Crop biologists are making concerted efforts to understand the stress adaptive mechanisms with an ultimate goal of manipulating specific traits to sustain production. In crop plants, drought tolerance is regulated by multiple traits among which the ones related to water relations and cellular tolerance are considered to be vital. The stress adaptive responses originate from the differential expression of genes, which are governed by complex regulatory networks. Modern research findings have revealed that small RNAs (sRNAs) such as microRNA and small-interfering RNA play crucial roles in plant stress adaptation. Recent studies demonstrated that leaf cuticle and surface wax serves as an important trait for multiple stress tolerance, and many regulatory genes coordinate wax accumulation. This review attempts to compile the information on sRNAs, its role in regulating drought trait expression, with main focus on the cuticular resistance trait, epicuticular waxes (EW). This review also outlines the relevance of key transcriptional regulators involved in cuticular wax production and the potential role of EW in combined stress tolerance in plants. Overall, the review highlights the need of exploring sRNAs associated with EW-trait for targeted manipulation to sustain productivity of crop plants under combined stresses.

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References

  • Abe, H., Urao, T., Ito, T., Seki, M., Shinozaki, K., & Yamaguchi-Shinozaki, K. (2003). Arabidopsis AtMYC2 (bHLH) and AtMYB2 (MYB) function as transcriptional activators in abscisic acid signaling. The Plant Cell, 15, 63–78.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Adato, A., Mandel, T., Mintz-Oron, S., Venger, I., Levy, D., Yativ, M., et al. (2009). Fruit-surface flavonoid accumulation in tomato is controlled by a SlMYB12-regulated transcriptional network. PLoS Genetics, 5, e1000777.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Aharoni, A., Dixit, S., Jetter, R., Thoenes, E., van Arkel, G., & Pereira, A. (2004). The SHINE clade of AP2 domain transcription factors activates wax biosynthesis, alters cuticle properties, and confers drought tolerance when overexpressed in Arabidopsis. The Plant Cell, 16, 2463–2480.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Almeida, R., & Allshire, R. C. (2005). RNA silencing and genome regulation. Trends in Cell Biology, 15, 251–258.

    Article  CAS  PubMed  Google Scholar 

  • Alptekin, B., Langridge, P., & Budak, H. (2017). Abiotic stress miRNomes in the Triticeae. Functional & Integrative Genomics, 17, 145–170.

    Article  CAS  Google Scholar 

  • Ashwini, N., Sajeevan, R. S., Udayakumar, M., & Nataraja, K. N. (2016). Identification and characterization of OsWRKY72 variant in indica genotypes. Rice Science, 23, 297–305.

    Article  Google Scholar 

  • Axtell, M. J. (2013). Classification and comparison of small RNAs from plants. Annual Review of Plant Biology, 64, 137–159.

    Article  CAS  PubMed  Google Scholar 

  • Babitha, K. C., Ramu, S. V., Nataraja, K. N., Sheshshayee, M. S., & Udayakumar, M. (2015). EcbZIP60, a basic leucine zipper transcription factor from Eleusine coracana L. improves abiotic stress tolerance in tobacco by activating unfolded protein response pathway. Molecular Breeding, 35, 181.

    Article  CAS  Google Scholar 

  • Babitha, K. C., Ramu, S. V., Pruthvi, V., Mahesh, P., Nataraja, K. N., & Udayakumar, M. (2013). Co-expression of AtbHLH17 and AtWRKY28 confers resistance to abiotic stress in Arabidopsis. Transgenic Research, 22, 327–341.

    Article  CAS  PubMed  Google Scholar 

  • Bao, S. G., Shi, J. X., Luo, F., Ding, B., Hao, J. Y., Xie, X. D., et al. (2017). Overexpression of Sorghum WINL1 gene confers drought tolerance in Arabidopsis thaliana through the regulation of cuticular biosynthesis. Plant Cell, Tissue and Organ Culture, 128, 347–356.

    Article  CAS  Google Scholar 

  • Barrera-Figueroa, B. E., Gao, L., Diop, N. N., Wu, Z. G., Ehlers, J. D., Roberts, P. A., et al. (2011). Identification and comparative analysis of drought-associated microRNAs in two cowpea genotypes. BMC Plant Biology, 11, 127.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bartel, D. P. (2004). MicroRNAs: genomics, biogenesis, mechanism, and function. Cell, 116, 281–297.

    Article  CAS  PubMed  Google Scholar 

  • Baulcombe, D. (2004). RNA silencing in plants. Nature, 431, 356–363.

    Article  CAS  PubMed  Google Scholar 

  • Beisson, F., Koo, A. J., Ruuska, S., Schwender, J., Pollard, M., Thelen, J. J., et al. (2003). Arabidopsis genes involved in acyl lipid metabolism. A 2003 census of the candidates, a study of the distribution of expressed sequence tags in organs, and a web-based database. Plant Physiolology, 132, 681–697.

    Article  CAS  Google Scholar 

  • Bengtson, C., Larsson, S., & Liljenberg, C. (1978). Effects of water stress on cuticular transpiration rate and amount and composition of epicuticular wax in seedlings of six oat varieties. Physiologia Plantarum, 44, 319–324.

    Article  CAS  Google Scholar 

  • Bernard, A., & Joubes, J. (2013). Arabidopsis cuticular waxes: advances in synthesis, export and regulation. Progress in Lipid Research, 52, 110–129.

    Article  CAS  PubMed  Google Scholar 

  • Bi, H., Luang, S., Li, Y., Bazanova, N., Borisjuk, N., Hrmova, M., et al. (2017). Wheat drought-responsive WXPL transcription factors regulate cuticle biosynthesis genes. Plant Molecular Biology, 94, 15–32.

    Article  CAS  PubMed  Google Scholar 

  • Bondada, B., Oosterhuis, D. M., Murphy, J. B., & Kim, K. S. (1996). Effect of water stress on the epicuticular wax composition and ultrastructure of cotton (Gossypium hirsutum L.) leaf, bract, and boll. Environmental and Experimental Botany, 36, 61–67.

    Article  CAS  Google Scholar 

  • Borges, F., & Martienssen, R. A. (2015). The expanding world of small RNAs in plants. Nature Reviews Molecular Cell Biology, 16(12), 727–741.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Borsani, O., Zhu, J., Verslues, P. E., Sunkar, R., Zhu, J. K., et al. (2005). Endogenous siRNAs derived from a pair of natural cis-antisense transcripts regulate salt tolerance in Arabidopsis. Cell, 123, 1279–1291.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Broun, P., Poindexter, P., Osborne, E., Jiang, C. Z., & Riechmann, J. L. (2004). WIN1, a transcriptional activator of epidermal wax accumulation in Arabidopsis. Proceedings of National Academy of Sciences U S A, 101, 4706–4711.

    Article  CAS  Google Scholar 

  • Budak, H., Kantar, M., Bulut, R., & Akpinar, B. A. (2015). Stress responsive miRNAs and isomiRs in cereals. Plant Science, 235, 1–13.

    Article  CAS  PubMed  Google Scholar 

  • Cameron, K. D., Teece, M. A., & Smart, L. B. (2006). Increased accumulation of cuticular wax and expression of lipid transfer protein in response to periodic drying events in leaves of tree tobacco. Plant Physiology, 140, 176–183.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Carthew, R. W., & Sontheimer, E. J. (2009). Origins and mechanisms of miRNAs and siRNAs. Cell, 136, 642–655.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cernac, A., & Benning, C. (2004). WRINKLED1 encodes an AP2/EREB domain protein involved in the control of storage compound biosynthesis in Arabidopsis. The Plant Journal, 40, 575–585.

    Article  CAS  PubMed  Google Scholar 

  • Chen, W., Kastner, C., Nowara, D., Oliveira-Garcia, E., Rutten, T., Zhao, Y., et al. (2016). Host-induced silencing of Fusarium culmorum genes protects wheat from infection. Journal of Experimental Botany, 67, 4979–4991.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cominelli, E., Sala, T., Calvi, D., Gusmaroli, G., & Tonelli, C. (2008). Overexpression of the Arabidopsis AtMYB41 gene alters cell expansion and leaf surface permeability. The Plant Journal, 53, 53–64.

    Article  CAS  PubMed  Google Scholar 

  • Cramer, G. R., Urano, K., Delrot, S., Pezzotti, M., & Shinozaki, K. (2011). Effects of abiotic stress on plants: a systems biology perspective. BMC Plant Biology, 11, 163.

    Article  PubMed  PubMed Central  Google Scholar 

  • Dai, A. (2012). Increasing drought under global warming in observations and models. Nature Climate Change, 3, 52–58.

    Article  Google Scholar 

  • Dhanyalakshmi, K. H., Naika, M. B. N., Sajeevan, R. S., Mathew, O. K., Shafi, K. M., Sowdhamini, R., et al. (2016). An approach to function annotation for Proteins of Unknown Function (PUFs) in the transcriptome of Indian mulberry. PLoS ONE, 11, e0151323.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ding, Y., Tao, Y., & Zhu, C. (2013). Emerging roles of microRNAs in the mediation of drought stress response in plants. Journal of Experimental Botany, 64(11), 3077–3086.

    Article  CAS  PubMed  Google Scholar 

  • Djami-Tchatchou, A. T., Sanan-Mishra, N., Ntushelo, K., & Dubery, I. A. (2017). Functional roles of microRNAs in agronomically important plants potential as targets for crop improvement and protection. Frontiers in Plant Science, 8, 378.

    Article  PubMed  PubMed Central  Google Scholar 

  • Dunoyer, P., Himber, C., & Voinnet, O. (2005). Dicer-like 4 is required for RNA interference and produces the 21-nucleotide small interfering RNA component of the plant cell-to-cell silencing signal. Nature Genetics, 37, 1356–1360.

    Article  CAS  PubMed  Google Scholar 

  • Eigenbrode, S. D., & Espelie, K. E. (1995). Effects of plant epicuticular lipids on insect herbivores. Annual Review of Entomology, 40, 171–194.

    Article  Google Scholar 

  • Ferdous, J., Hussain, S. S., & Shi, B. J. (2015). Role of microRNAs in plant drought tolerance. Plant Biotechnology Journal, 13, 293–305.

    Article  CAS  PubMed  Google Scholar 

  • Fich, E. A., Segerson, N. A., & Rose, J. K. (2016). The plant polyester cutin: biosynthesis, structure, and biological roles. Annual Review of Plant Biology, 67, 207–233.

    Article  CAS  PubMed  Google Scholar 

  • Fire, A., Xu, S., Montgomery, M. K., Kostas, S. A., Driver, S. E., & Mello, C. C. (1998). Potent and specific genetic interference by double-stranded RNA in Caenorhabditis elegans. Nature, 391, 806–811.

    Article  CAS  PubMed  Google Scholar 

  • Gahlaut, V., Jaiswal, V., Kumar, A., & Gupta, P. K. (2016). Transcription factors involved in drought tolerance and their possible role in developing drought tolerant cultivars with emphasis on wheat (Triticum aestivum L.). Theoretical and Applied Genetics, 129(11), 2019–2042.

    Article  CAS  PubMed  Google Scholar 

  • Gasciolli, V., Mallory, A. C., Bartel, D. P., & Vaucheret, H. (2005). Partially redundant functions of Arabidopsis dicer-like enzymes and a role for DCL4 in producing trans-acting siRNAs. Current Biology, 15, 1494–1500.

    Article  CAS  PubMed  Google Scholar 

  • Gilding, E. K., & Marks, M. D. (2010). Analysis of purified glabra 3-shapeshifter trichomes reveals a role for NOECK in regulating early trichome morphogenic events. The Plant Journal, 64, 304–317.

    Article  CAS  PubMed  Google Scholar 

  • Go, Y. S., Kim, H., Kim, H. J., & Suh, M. C. (2014). Arabidopsis cuticular wax biosynthesis is negatively regulated by the DEWAX gene encoding an AP2/ERF-type transcription factor. The Plant Cell, 26, 1666–1680.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Grosshans, H., & Filipowicz, W. (2008). Molecular biology: the expanding world of small RNAs. Nature, 451, 414–416.

    Article  CAS  PubMed  Google Scholar 

  • Guleria, P., Mahajan, M., Bhardwaj, J., & Yadav, S. K. (2011). Plant small RNAs: Biogenesis, mode of action and their roles in abiotic stresses. Genomics Proteomics Bioinformatics, 9(9), 183–199.

    Article  CAS  PubMed  Google Scholar 

  • Guo, L., Yang, H., Zhang, X., & Yang, S. (2013). Lipid transfer protein 3 as a target of MYB96 mediates freezing and drought stress in Arabidopsis. Journal of Experimental Botany, 64, 1755–1767.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hadiarto, T., & Tran, L. S. (2011). Progress studies of drought-responsive genes in rice. Plant Cell Reports, 30(3), 297–310.

    Article  CAS  PubMed  Google Scholar 

  • Hamilton, A. J., & Baulcombe, D. C. (1999). A novel species of small anti-sense RNA in posttranscriptional gene silencing. Science, 286, 950–952.

    Article  CAS  PubMed  Google Scholar 

  • Hamilton, A., Voinnet, O., Chappell, L., & Baulcombe, D. (2002). Two classes of short interfering RNA in RNA silencing. EMBO Journal, 21, 4671–4679.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hao, S., Ma, Y., Zhao, S., Ji, Q., Zhang, K., Yang, M., et al. (2017). McWRI1, a transcription factor of the AP2/SHEN family, regulates the biosynthesis of the cuticular waxes on the apple fruit surface under low temperature. PLoS ONE, 12(10), e0186996.

    Article  PubMed  PubMed Central  Google Scholar 

  • Hilbricht, T., Varotto, S., Sgaramella, V., Bartels, D., Salamini, F., & Furini, A. (2008). Retrotransposons and siRNA have a role in the evolution of desiccation tolerance leading to resurrection of the plant Craterostigma plantagineum. New Phytologist, 179, 877–887.

    Article  CAS  PubMed  Google Scholar 

  • Hirel, B., Le Gouis, J., Ney, B., & Gallais, A. (2007). The challenge of improving nitrogen use efficiency in crop plants: towards a more central role for genetic variability and quantitative genetics within integrated approaches. Journal of Experimental Botany, 58, 2369–2387.

    Article  CAS  PubMed  Google Scholar 

  • Hoang, M. H., Nguyen, X. C., Lee, K., Kwon, Y. S., Pham, H. T., Park, H. C., et al. (2012). Phosphorylation by ATMPK6 is required for the biological function of AtMYB41 in Arabidopsis. Biochemical and Biophysical Research Communications, 422, 181–186.

    Article  CAS  PubMed  Google Scholar 

  • Huang, D., Feurtado, J. A., Smith, M. A., Flatman, L. K., Koh, C., & Cutler, A. J. (2017). Long noncoding miRNA gene represses wheat β-diketone waxes. Proceedings of National Academy of Sciences U S A, 114(15), E3149–E3158.

    Article  CAS  Google Scholar 

  • Islam, M. A., Du, H., Ning, J., Ye, H., & Xiong, L. (2009). Characterization of Glossy1-homologous genes in rice involved in leaf wax accumulation and drought resistance. Plant Molecular Biology, 70, 443–456.

    Article  CAS  PubMed  Google Scholar 

  • Javelle, M., Vernoud, V., Depege-Fargeix, N., Arnould, C., Oursel, D., Domergue, F., et al. (2010). Overexpression of the epidermis-specific homeodomain-leucine zipper IV transcription factor outer cell layer1 in maize identifies target genes involved in lipid metabolism and cuticle biosynthesis. Plant Physiology, 154, 273–286.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jefferson, P., Johnson, D., Rumbaugh, M., & Asay, K. (1989). Water stress and genotypic effects on epicuticular wax production of alfalfa and crested wheatgrass in relation to yield and excised leaf water loss rate. Canadian Journal of Plant Science, 69, 481–490.

    Article  Google Scholar 

  • Jenks, M. A., Andersen, L., Teusink, R. S., & Williams, M. H. (2001). Leaf cuticular waxes of potted rose cultivars as affected by plant development, drought and paclobutrazol treatments. Physiologia Plantarum, 112, 62–70.

    Article  CAS  PubMed  Google Scholar 

  • Jenks, M. A., Joly, R. J., Peters, P. J., Rich, P. J., Axtell, J. D., & Ashworth, E. N. (1994). Chemically induced cuticle mutation affecting epidermal conductance to water vapor and disease susceptibility in Sorghum bicolor (L.) Moench. Plant Physiology, 105, 1239–1245.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jetter, R., & Kunst, L. (2008). Plant surface lipid biosynthetic pathways and their utility for metabolic engineering of waxes and hydrocarbon biofuels. The Plant Journal, 54, 670–683.

    Article  CAS  PubMed  Google Scholar 

  • Jetter, R., Kunst, L., & Samuels, A. L. (2006). Composition of plant cuticular waxes. In M. Riederer & C. Müller (Eds.), Annual plant reviews 23: Biology of the Plant cuticle (pp. 145–181). Oxford: Blackwell Publishing.

    Chapter  Google Scholar 

  • Jin, D., Wang, Y., Zhao, Y., & Chen, M. (2013). MicroRNAs and their cross-talks in plant development. Journal of Genetics and Genomics, 40(4), 161–170.

    Article  CAS  PubMed  Google Scholar 

  • Jordan, W., Shouse, P. J., Blum, A., Miller, F. R., & Monk, R. L. (1984). Environmental physiology of sorghum. II. Epicuticular wax load and cuticular transpiration. Crop Science, 24, 1168–1173.

    Article  Google Scholar 

  • Joshi, R., Wani, S. H., Singh, B., Bohra, A., Dar, Z. A., Lone, A. A., et al. (2016). Transcription factors and plants response to drought stress: current understanding and future directions. Frontiers in Plant Science, 7, 1029.

    Article  PubMed  PubMed Central  Google Scholar 

  • Ju, S., Go, Y. S., Choi, H. J., Park, J. M., & Suh, M. C. (2017). DEWAX transcription factor is involved in resistance to Botrytis cinerea in Arabidopsis thaliana and Camelina sativa. Frontiers Plant Science, 8, 1210.

    Article  Google Scholar 

  • Juliano, C., Wang, J., & Lin, H. (2011). Uniting germline and stem cells: the function of Piwi proteins and the piRNA pathway in diverse organisms. Annual Review of Genetics, 45, 447–469.

    Article  CAS  PubMed  Google Scholar 

  • Kannangara, R., Branigan, C., Liu, Y., Penfield, T., Rao, V., Mouille, G., et al. (2007). The transcription factor WIN1/SHN1 regulates cutin biosynthesis in Arabidopsis thaliana. The Plant Cell, 19(4), 1278–1294.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Karaba, A., Dixit, S., Greco, R., Aharoni, A., Trijatmiko, K. R., Marsch-Martinez, N., et al. (2007). Improvement of water use efficiency in rice by expression of HARDY, an Arabidopsis drought and salt tolerance gene. Proceedings of National Academy of Sciences U S A, 104, 15270–15275.

    Article  CAS  Google Scholar 

  • Kathuria, K., Giri, J., Nataraja, K. N., Murata, N., Udayakumar, M., & Tyagi, A. K. (2009). Glycine betaine-induced water stress tolerance in codA-expressing transgenic indica rice is associated with up-regulation of several stress responsive genes. Plant Biotechnology Journal, 7, 512–526.

    Article  CAS  PubMed  Google Scholar 

  • Kerstiens, G. (Ed.). (1996). Plant cuticles: An integrated functional approach. Oxford, UK: BIOS Scientific Publishers Limited.

    Google Scholar 

  • Kim, V. N. (2005). Small RNAs: Classification, biogenesis, and function. Molecules and Cells, 19, 01–15.

    CAS  Google Scholar 

  • Kim, J. M., To, K. T., Matsui, A., Tanoi, K., Kobayashi, N. I., Matsuda, F., et al. (2017). Acetate-mediated novel survival strategy against drought in plants. Nature Plants, 3, 17097.

    Article  CAS  PubMed  Google Scholar 

  • Kosma, D. K., Bourdenx, B., Bernard, A., Parsons, E. P., Lu, S., Joubes, J., et al. (2009). The impact of water deficiency on leaf cuticle lipids of Arabidopsis. Plant Physiology, 151, 1918–1929.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Krannich, C. T., Maletzki, L., Kurowsky, C., & Horn, R. (2015). Network candidate genes in breeding for drought tolerant crops. International Journal of Molecular Sciences, 16(7), 16378–16400.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ku, Y. S., Wong, J. W. H., Mui, Z., Liu, X., Hui, J. H. L., & Chan, T. F. (2015). Small RNAs in plant responses to abiotic stresses: Regulatory roles and study methods. International Journal of Molecular Sciences, 16, 24532–24554.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kumar, R. (2014). Role of microRNAs in biotic and abiotic stress responses in crop plants. Applied Biochemistry and Biotechnology, 174, 93–115.

    Article  CAS  PubMed  Google Scholar 

  • Kunst, L., & Samuels, A. L. (2003). Biosynthesis and secretion of plant cuticular wax. Progress in Lipid Research, 42, 51.

    Article  CAS  PubMed  Google Scholar 

  • Lam, P., Zhao, L., Eveleigh, N., Yu, Y., Kn, C., & Kunst, (2015). The exosome and trans-acting small interfering RNAs Regulate cuticular wax biosynthesis during Arabidopsis inflorescence stem development. Plant Physiology, 167, 323–336.

    Article  CAS  PubMed  Google Scholar 

  • Lee, S. B., Kim, H. U., & Suh, M. C. (2016). MYB94 and MYB96 additively activate cuticular wax biosynthesis in Arabidopsis. Plant and Cell Physiology, 57(11), 2300–2311.

    Article  CAS  PubMed  Google Scholar 

  • Lee, S. B., & Suh, M. C. (2015a). Advances in the understanding of cuticular waxes in Arabidopsis thaliana and crop species. Plant Cell Reports, 34, 557–572.

    Article  CAS  PubMed  Google Scholar 

  • Lee, S. B., & Suh, M. C. (2015b). Cuticular wax biosynthesis is up-regulated by the MYB94 transcription factor in Arabidopsis. Plant and Cell Physiology, 56, 48–60.

    Article  CAS  PubMed  Google Scholar 

  • Lesk, C., Rowhani, P., & Ramankutty, N. (2016). Influence of extreme weather disasters on global crop production. Nature, 529, 84–87.

    Article  CAS  PubMed  Google Scholar 

  • Li, W. X., Oono, Y., Zhu, J., He, X. J., Wu, J. M., Iida, K., et al. (2008). The Arabidopsis NFYA5 transcription factor is regulated transcriptionally and post transcriptionally to promote drought resistance. The Plant Cell, 20, 2238–2251.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li-Beisson, Y., Shorrosh, B., Beisson, F., Andersson, M. X., Arondel, V., Bates, P. D., et al. (2013). Acyl-lipid metabolism. Arabidopsis Book, 8, e0161.

    Article  Google Scholar 

  • Lisso, J., Schroder, F., Schippers, J. H., & Mussig, C. (2012). NFXL2 modifies cuticle properties in Arabidopsis. Plant Signal & Behavior, 7, 551–555.

    Article  CAS  Google Scholar 

  • Liu, Q., & Chen, Y. Q. (2010). A new mechanism in plant engineering: the potential roles of microRNAs in molecular breeding for crop improvement. Biotechnology Advances, 28, 301–307.

    Article  CAS  PubMed  Google Scholar 

  • Liu, H., Tian, X., Li, Y., Wu, C. A., & Zheng, C. (2008). Microarray-based analysis of stress-regulated microRNAs in Arabidopsis thaliana. RNA, 14, 836–843.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Long, L. M., Patel, H. P., Cory, W. C., & Stapleton, A. E. (2003). The maize epicuticular wax layer provides UV protection. Functional Plant Biology, 30, 75–81.

    Article  Google Scholar 

  • Mamrutha, H. M., Mogili, T., Lakshmi, J. K., Rama, N., Kosma, D., Udaya Kumar, M., et al. (2010). Leaf cuticular wax amount and crystal morphology regulate post-harvest water loss in mulberry (Morus species). Plant Physiology and Biochemistry, 48, 690–696.

    Article  CAS  PubMed  Google Scholar 

  • Mamrutha, H. M., Nataraja, K. N., Rama, N., Kosma, D. K., Mogili, T., Jhansi-Lakshmi, K., et al. (2017). Leaf surface wax composition of genetically diverse mulberry (Morus sp.) genotypes and its close association with expression of genes involved in wax metabolism. Current Science, 112, 759–766.

    Article  Google Scholar 

  • Masaki, T., Mitsui, N., Tsukagoshi, H., Nishii, T., Morikami, A., & Nakamura, K. (2005). ACTIVATOR of spomin:LUC1/WRINKLED1 of Arabidopsis thaliana trans-activates sugar-inducible promoters. Plant and Cell Physiology, 46, 547–556.

    Article  CAS  PubMed  Google Scholar 

  • McFarlane, H. E., Watanabe, Y., Yang, W., Huang, Y., Ohlrogge, J., & Samuels, A. L. (2014). Golgi- and trans-Golgi network-mediated vesicle trafficking is required for wax secretion from epidermal cells. Plant Physiology, 164(3), 1250–1260.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Meena, K. K., Sorty, A. M., Bitla, U. M., Choudhary, K., Gupta, P., Pareek, A., et al. (2017). Abiotic stress responses and microbe-mediated mitigation in plants: the omics strategies. Frontiers in Plant Science, 8, 172.

    Article  PubMed  PubMed Central  Google Scholar 

  • Mintz-Oron, S., Mandel, T., Rogachev, I., Feldberg, L., Lotan, O., Yativ, M., et al. (2008). Gene expression and metabolism in tomato fruit surface tissues. Plant Physiology, 147, 823–851.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mirouze, M., & Paszkowski, J. (2011). Epigenetic contribution to stress adaptation in plants. Current Opinion in Plant Biology, 14, 267–274.

    Article  CAS  PubMed  Google Scholar 

  • Moldovan, D., Spriggs, A., Yang, J., Pogson, B. J., Dennis, E. S., & Wilson, I. W. (2010). Hypoxia-responsive microRNAs and trans-acting small interfering RNAs in Arabidopsis. Journal of Experimental Botany, 61, 165–177.

    Article  CAS  PubMed  Google Scholar 

  • Nadakuduti, S. S., Pollard, M., Kosma, D. K., Allen, C., Jr., Ohlrogge, J. B., & Barry, C. S. (2012). Pleiotropic phenotypes of the sticky peel mutant provide new insight into the role of CUTIN DEFICIENT2 in epidermal cell function in tomato. Plant Physiology, 159, 945–960.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nagahatenna, D. S., Langridge, P., & Whitford, R. (2015). Tetrapyrrole-based drought stress signalling. Plant Biotechnology Journal, 13(4), 447–459.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nagarjuna, K. N., Parvathi, M. S., Sajeevan, R. S., Pruthvi, V., Mamrutha, H. M., & Nataraja, K. N. (2016). Full-length cloning and characterization of abiotic stress responsive CIPK31-like gene from finger millet, a drought-tolerant crop. Current Science, 111, 890.

    Article  CAS  Google Scholar 

  • Nagaveni, N., Rama, N., Jayaraman, R., Viswanathan, C., & Nataraja, K. N. (2016). Ectopic expression of AtICE1 and OsICE1 transcription factor delays stress-induced senescence and improves tolerance to abiotic stresses in tobacco. Journal of Plant Biochemistry and Biotechnology, 25, 285–293.

    Article  CAS  Google Scholar 

  • Navarro, M., Ayax, C., Martinez, Y., Laur, J., El Kayal, W., Marque, C., et al. (2011). Two EguCBF1 genes overexpressed in Eucalyptus display a different impact on stress tolerance and plant development. Plant Biotechnology Journal, 9, 50–63.

    Article  CAS  PubMed  Google Scholar 

  • Nawrath, C., Schreiber, L., Franke, R. B., Geldner, N., Reina-Pinto, J. J., & Kunst, L. (2013). Apoplastic diffusion barriers in Arabidopsis. The Arabidopsis Book/American Society of Plant Biologists, 11, e0167.

    PubMed Central  Google Scholar 

  • Oshima, Y., & Mitsuda, N. (2013). The MIXTA-like Transcription factor MYB16 is a major regulator of cuticle formation in vegetative organs. Plant Signal & Behavior, 9, e26826.

    Article  CAS  Google Scholar 

  • Oshima, Y., Shikata, M., Koyama, T., Ohtsubo, N., Mitsuda, N., & Ohme-Takagi, M. (2013). MIXTA-like transcription factors and WAX INDUCER1/SHINE1 coordinately regulate cuticle development in Arabidopsis and Torenia fournieri. The Plant Cell, 25, 1609–1624.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Park, C. S., Go, Y. S., & Suh, M. C. (2016). Cuticular wax biosynthesis is positively regulated by WRINKLED4, an AP2/ERF-type transcription factor, in Arabidopsis stems. The Plant Journal, 88, 257–270.

    Article  CAS  PubMed  Google Scholar 

  • Parvathi, M. S., & Nataraja, K. N. (2016). Emerging tools, concepts and ideas to track the modulator genes underlying plant drought adaptive traits: An overview. Plant Signaling Behaviour, 11(1), e1074370.

    Article  CAS  Google Scholar 

  • Parvathi, M. S., & Nataraja, K. N. (2017a). Simultaneous expression of abiotic stress-responsive genes: An approach to improve multiple stress tolerance in crops. In M. Senthil-Kumar (Ed.), Plant tolerance to individual and concurrent stresses (pp. 151–163). New Delhi: Springer.

  • Parvathi, M. S., & Nataraja, K. N. (2017b). Discovery of stress responsive TATA-box binding protein associated Factor6 (TAF6) from finger millet (Eleusine coracana (L.) Gaertn). Journal of Plant Biology, 60(4), 335–342.

    Article  CAS  Google Scholar 

  • Parvathi, M. S., Nataraja, K. N., Yashoda, B. K., Ramegowda, H. V., Mamrutha, H. M., & Rama, N. (2013). Expression analysis of stress responsive pathway genes linked to drought hardiness in an adapted crop, finger millet (Eleusine coracana). Journal of Plant Biochemistry and Biotechnology, 22(2), 193–201.

    Article  CAS  Google Scholar 

  • Pruthvi, V., Narasimhan, R., & Nataraja, K. N. (2014). Simultaneous expression of abiotic stress responsive transcription factors, AtDREB2A, AtHB7 and AtABF3 improves salinity and drought tolerance in peanut (Arachis hypogaea L.). PLoS ONE, 9, 1–21.

    Article  CAS  Google Scholar 

  • Pruthvi, V., Rama, N., Govind, G., & Karaba, N. K. (2013). Expression analysis of drought specific genes in peanut (Arachis hypogaea, L.). Physiology and Molecular Biology of Plants, 19, 277–281.

    Article  CAS  PubMed  Google Scholar 

  • Pruthvi, V., Rama, N., Parvathi, M. S., & Nataraja, K. N. (2017). Transgenic tobacco plants constitutively expressing peanut BTF3 exhibit increased growth and tolerance to abiotic stresses. Plant Biology, 19(3), 377–385.

    Article  CAS  PubMed  Google Scholar 

  • Ramegowda, V., Gill, U. S., Sivalingam, P. N., Gupta, A., Gupta, C., Govind, K., et al. (2017). GBF3 transcription factor imparts drought tolerance in Arabidopsis thaliana. Scientific Reports, 7, 9148.

    Article  PubMed  PubMed Central  Google Scholar 

  • Ramegowda, V., Senthil-Kumar, M., Nataraja, K. N., Reddy, M. K., Mysore, K. S., & Udayakumar, M. (2012). Expression of a finger millet transcription factor, EcNAC1, in tobacco confers abiotic stress-tolerance. PLoS ONE, 7, 40397.

    Article  CAS  Google Scholar 

  • Rashotte, A. M., Jenks, M. A., Nguyen, T. D., & Feldmann, K. A. (1997). Epicuticular wax variation in ecotypes of Arabidopsis thaliana. Phytochemistry, 45(2), 251–255.

    Article  CAS  PubMed  Google Scholar 

  • Reinhart, B. J., Weinstein, E. G., Rhoades, M. W., Bartel, B., & Bartel, D. P. (2002). MicroRNAs in plants. Genes & Development, 16, 1616–1626.

    Article  CAS  Google Scholar 

  • Reyes, J. L., & Chua, N. H. (2007). ABA induction of miR159 controls transcript levels of two MYB factors during Arabidopsis seed germination. The Plant Journal, 49, 592–606.

    Article  CAS  PubMed  Google Scholar 

  • Sajeevan, R. S., & Nataraja, K. N. (2016). Molecular cloning and characterization of a novel basic helix–loop–helix-144 (bHLH144)-like transcription factor from Morus alba (L.). Plant Gene, 5, 109–117.

    Article  CAS  Google Scholar 

  • Sajeevan, R. S., Nataraja, K. N., Shivashankara, K. S., Pallavi, N., Gurumurthy, D. S., & Shivanna, M. B. (2017). Expression of Arabidopsis SHN1 in Indian Mulberry (Morus indica L.) increases leaf surface wax content and reduces post-harvest water loss. Frontiers Plant Science, 8, 418.

    Article  CAS  Google Scholar 

  • Samdur, M., Manivel, P., Jain, V. B., Chikani, B. M., Gor, H. K., Desai, S., et al. (2003). Genotypic differences and water-deficit induced enhancement in epicuticular wax load in peanut. Crop Science, 43, 1294–1299.

    Article  Google Scholar 

  • Samuels, L., DeBono, A., Lam, P., Wen, M., Jetter, R., & Kunst, L. (2008). Use of Arabidopsis eceriferum mutants to explore plant cuticle biosynthesis. Journal of Visualized Experiments, 31, 709.

    Google Scholar 

  • Seo, P. J., Lee, S. B., Suh, M. C., Park, M. J., Go, Y. S., & Park, C. M. (2011). The MYB96 transcription factor regulates cuticular wax biosynthesis under drought conditions in Arabidopsis. The Plant Cell, 23, 1138–1152.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Seo, P. J., & Park, C. M. (2010). MYB96-mediated abscisic acid signals induce pathogen resistance response by promoting salicylic acid biosynthesis in Arabidopsis. New Phytologist, 186, 471–483.

    Article  CAS  PubMed  Google Scholar 

  • Seo, P. J., & Park, C. M. (2011). Cuticular wax biosynthesis as a way of inducing drought resistance. Plant Signal & Behavior, 6, 1043–1045.

    Article  CAS  Google Scholar 

  • Seo, P. J., Xiang, F., Qiao, M., Park, J. Y., Lee, Y. N., Kim, S. G., et al. (2009). The MYB96 transcription factor mediates abscisic acid signaling during drought stress response in Arabidopsis. Plant Physiology, 151, 275–289.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Serrano, M., Coluccia, F., Torres, M., L’Haridon, F., & Métraux, J. P. (2014). The cuticle and plant defense to pathogens. Frontiers in Plant Science, 5, 274.

    Article  PubMed  PubMed Central  Google Scholar 

  • Shi, J. X., Adato, A., Alkan, N., He, Y., Lashbrooke, J., Matas, A. J., et al. (2013). The tomato SlSHINE3 transcription factor regulates fruit cuticle formation and epidermal patterning. New Phytologist, 197, 468–480.

    Article  CAS  PubMed  Google Scholar 

  • Shi, J. X., Malitsky, S., De Oliveira, S., Branigan, C., Franke, R. B., Schreiber, L., et al. (2011). SHINE transcription factors act redundantly to pattern the archetypal surface of Arabidopsis flower organs. PLoS Genetics, 7, e1001388.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sunkar, R., Chinnusamy, V., Zhu, J., & Zhu, J. K. (2007). Small RNAs as big players in plant abiotic stress responses and nutrient deprivation. Trends in Plant Science, 12, 301–309.

    Article  CAS  PubMed  Google Scholar 

  • Sunkar, R., & Zhu, J. K. (2004). Novel and stress-regulated microRNAs and other small RNAs from Arabidopsis. The Plant Cell, 16, 2001–2019.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sunkar, R., & Zhu, J. K. (2007). Micro RNAs and short-interfering RNAs in plants. Journal of Integrative Plant Biology, 49, 817–826.

    Article  CAS  Google Scholar 

  • Taketa, S., Amano, S., Tsujino, Y., Sato, T., Saisho, D., Kakeda, K., et al. (2008). Barley grain with adhering hulls is controlled by an ERF family transcription factor gene regulating a lipid biosynthesis pathway. Proceedings of National Academy of Sciences U S A, 105, 4062–4067.

    Article  CAS  Google Scholar 

  • Tiwari, M., Sharma, D., & Trivedi, P. K. (2014). Artificial microRNA mediated gene silencing in plants: progress and perspectives. Plant Molecular Biology, 86, 1–18.

    Article  CAS  PubMed  Google Scholar 

  • To, A., Joubes, J., Barthole, G., Lecureuil, A., Scagnelli, A., Jasinski, S., et al. (2012). WRINKLED transcription factors orchestrate tissue-specific regulation of fatty acid biosynthesis in Arabidopsis. The Plant Cell, 24, 5007–5023.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tuberosa, R. (2012). Phenotyping for drought tolerance of crops in the genomics era. Frontiers in Physiology, 3, 347.

    Article  PubMed  PubMed Central  Google Scholar 

  • Vaucheret, H. (2006). Post-transcriptional small RNA pathways in plants: Mechanism and regulations. Genes & Development, 20, 759–771.

    Article  CAS  Google Scholar 

  • Wang, Y., Wan, L., Zhang, L., Zhang, Z., Zhang, H., Quan, R., et al. (2012). An ethylene response factor OsWR1 responsive to drought stress transcriptionally activates wax synthesis related genes and increases wax production in rice. Plant Molecular Biology, 78, 275–288.

    Article  CAS  PubMed  Google Scholar 

  • Watanabe, T., Totoki, Y., Sasaki, H., Minami, N., & Imai, H. (2007). Analysis of small RNA profiles during development. Methods in Enzymology, 427, 155–169.

    Article  CAS  PubMed  Google Scholar 

  • Wu, R., Li, S., He, S., Wassmann, F., Yu, C., Qin, G., et al. (2011). CFL1, a WW domain protein, regulates cuticle development by modulating the function of HDG1, a class IV homeodomain transcription factor, in rice and Arabidopsis. The Plant Cell, 23, 3392–3411.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xia, K., Ou, X., Gao, C., Tang, H., Jia, Y., Deng, R., et al. (2015). OsWS1 involved in cuticular wax biosynthesis is regulated by osa-miR1848. Plant, Cell and Environment, 38, 2662–2673.

    Article  CAS  PubMed  Google Scholar 

  • Xie, Z., Johansen, L. K., Gustafson, A. M., Kasschau, K. D., Lellis, A. D., Zilberman, D., et al. (2004). Genetic and functional diversification of small RNA pathways in plants. PLoS Biology, 2, E104.

    Article  PubMed  PubMed Central  Google Scholar 

  • Yang, J., Zhao, X., Liang, L., Xia, Z., Lei, L., Niu, X., et al. (2011). Overexpression of a cuticle-degrading protease Ver112 increases the nematicidal activity of Paecilomyces lilacinus. Applied Microbiology and Biotechnology, 89, 1895–1903.

    Article  CAS  PubMed  Google Scholar 

  • Yeats, T. H., & Rose, J. K. C. (2008). The biochemistry and biology of extracellular plant lipid-transfer proteins (LTPs). Protein Science, 17, 191–198.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang, J. Y., Broeckling, C. D., Blancaflor, E. B., Sledge, M. K., Sumner, L. W., & Wang, Z. Y. (2005). Overexpression of WXP1, a putative Medicago truncatula AP2 domain-containing transcription factor gene, increases cuticular wax accumulation and enhances drought tolerance in transgenic alfalfa (Medicago sativa). The Plant Journal, 42, 689–707.

    Article  CAS  PubMed  Google Scholar 

  • Zhang, J. Y., Broeckling, C. D., Sumner, L. W., & Wang, Z. Y. (2007). Heterologous expression of two Medicago truncatula putative ERF transcription factor genes, WXP1 and WXP2, in Arabidopsis led to increased leaf wax accumulation and improved drought tolerance, but differential response in freezing tolerance. Plant Molecular Biology, 64, 265–278.

    Article  CAS  PubMed  Google Scholar 

  • Zhang, Z., Wei, L., Zou, X., Tao, Y., Liu, Z., & Zheng, Y. (2008). Submergence-responsive microRNAs are potentially involved in the regulation of morphological and metabolic adaptations in Maize Root Cells. Annals of Botany, 102, 509–519.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhao, L., & Kunst, L. (2016). SUPERKILLER complex components are required for the RNA exosome-mediated control of cuticular wax biosynthesis in Arabidopsis inflorescence stems. Plant Physiology, 171, 960–973.

    PubMed  PubMed Central  Google Scholar 

  • Zhao, B., Liang, R., Ge, L., Li, W., Xiao, H., Lin, H., et al. (2007). Identification of drought-induced microRNAs in rice. Biochemical and Biophysical Research Communications, 354, 585–590.

    Article  CAS  PubMed  Google Scholar 

  • Zhou, X., Jenks, M. A., Liu, J., Liu, A., Zhang, X., Xiang, J., et al. (2014). Overexpression of transcription factor OsWR2 regulates wax and cutin biosynthesis in rice and enhances its tolerance to water deficit. Plant Molecular Biology Reports, 32, 719–731.

    Article  CAS  Google Scholar 

  • Zhou, L., Liu, Y., Liu, Z., Kong, D., Duan, M., & Luo, L. (2010). Genome-wide identification and analysis of drought-responsive microRNAs in Oryza sativa. Journal of Experimental Botany, 61, 4157–4168.

    Article  CAS  PubMed  Google Scholar 

  • Zilberman, D., Cao, X., & Jacobsen, S. E. (2003). Argonaute4 control of locus-specific siRNA accumulation and DNA and histone methylation. Science, 299, 716–719.

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

We would like to thank the Directorate of Research, University of Agricultural Sciences, GKVK, Bengaluru for the research grant (Ref. number: DR/Prof.(S)/RKVY/B-44/2017–18).

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Correspondence to Karaba N. Nataraja.

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Sajeevan, R.S., Parvathi, M.S. & Nataraja, K.N. Leaf wax trait in crops for drought and biotic stress tolerance: regulators of epicuticular wax synthesis and role of small RNAs. Ind J Plant Physiol. 22, 434–447 (2017). https://doi.org/10.1007/s40502-017-0333-9

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