sRNA and epigenetic


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sRNA and epigenetic mediated abiotic stress tolerance in plants:


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123 Indian Journal of Plant Physiology An International Journal of Plant Physiology ISSN 0019-5502 Volume 22 Number 4 Ind J Plant Physiol. 2017 22:458-469 DOI 10.1007/s40502-017-0330-z sRNA and epigenetic mediated abiotic stress tolerance in plants Monika Saroha Garima Singroha Manisha Sharma Geetika Mehta Om Prakash Gupta Pradeep Sharma

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REVIEW ARTICLE sRNA and epigenetic mediated abiotic stress tolerance in plants Monika Saroha 1 • Garima Singroha 1 • Manisha Sharma 1 • Geetika Mehta 1 • Om Prakash Gupta 1 • Pradeep Sharma 1 Received: 4 November 2017/Accepted: 13 November 2017/Published online: 22 December 2017 Indian Society for Plant Physiology 2017 Abstract Plant small RNAs are important regulators of gene expression involved in epigenetic processes under abiotic and biotic stresses. To minimize the stress influ- ence specific changes in gene expression are induced that could be epigenetically without changing DNA sequence fixed and passed into off springs forming epigenetic memories. sRNAs are crucial regulators of endogenous gene expression at both transcriptional and post transcrip- tional levels. The use of high throughput sequencing techniques bioinformatics and computational tools lead to identification and characterization of various stress asso- ciated sRNAs and their target genes in plants. This review focuses on various epigenetic processes involved stress response and the roles of various sRNAs involved in abi- otic stress tolerance in plants. Keywords sRNA Epigenetics Abiotic stress Salinity Drought Heat Introduction Small RNAs are short 20–30 nucleotides and endogenous RNAs that are either encoded in cis or in trans fashion and are primarily associated with post transcrip- tional gene regulations Budak et al. 2015. cis encoded sRNAs are transcribed from their target mRNA’s antisense strand due to which these are perfectly complementary whereas trans- encoded sRNAs have only limited complementarity Gottesman 2005.SmallRNAsbelongto two major classes on the basis of their biogenesis and precursor structure microRNAs miRNAs and endoge- nous short-interfering RNAs siRNAs. The plant miRNAs are generated by endonucleolytic processing from 64 to 303 nt long single stranded hairpin precursors by the enzyme dicer. The hairpin precursor RNAs are transcribed from endogenous non protein-coding genes Ambros 2004 Bartel 2004. miRNA silences genes post transcriptionally by targeting mRNA for degradation or repressing transla- tion Mallory etal.2004.siRNAsareabout20–25 ntlong which are also processed by dicer. These may be either exogenous or endogenous in origin. They are quite similar to miRNAs but their origin mode of action structure and associated proteins vary from each other Bartel 2004 Carthew and Sontheimer 2009. siRNAs are related with both post-transcriptional gene silencing and transcriptional gene silencing involving chromatin remodeling Finnegan and Matzke 2003. siRNA are generated from dsRNAs due to antisense or convergent transcription or due to the activity of one or more cellular RNA-dependent RNA polymerases RdRPs Baulcombe 2004. These can often direct DNA methylation at target sequences. sRNAs do not code for proteins but instead interrupt mRNA translation thereby silencing the gene expression Borsani et al. 2005 Vazquez 2006. They inhibit gene expression by employing a non-catalytic mechanism of action by base-pairing with target mRNAs thus interfering the ribosome binding and inhibiting target mRNA trans- lation Morita et al. 2006. These tiny RNAs are also involved in regulation of gene expression through DNA methylation Baulcombe 2004 in many biological pro- cesses ranging from developmental processes to biotic and abiotic stress response Kamthan et al. 2015. Plants experience various abiotic stresses such as high/low Pradeep Sharma 1 ICAR-IndianInstituteofWheat andBarleyResearch Karnal India 123 Ind J Plant Physiol. October–December 2017 224:458–469 Authors personal copy

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temperatures drought/water lodging salinity nutrient deficiency and oxidative stress etc. These stress condi- tions trigger a diverse set of physiological metabolic and defense related genes which helps in sustaining the growth of the plant. It has been observed that stress can decrease the yield of major crop plants by 50 Rodriguez et al. 2005. It has been observed that sRNA play an important role in response to various abiotic and biotic stresses and have the potential to serve as promising candidates for developing transgenic plants against stresses. With the initiation of epigenetic regulatory mechanisms studies on gene regulation by small RNAs and alteration in methy- lation status during adverse environmental conditions have also been done. Epigenetic regulation of abiotic stress in plants Plants manipulate their existing genetic information to compensate the exposure to adverse conditions. This involves modifications of gene expression without chang- ing original DNA sequence known as epigenetics Whitelaw and Whitelaw 2006. This can be achieved by reversible DNA methylation histone modifications acetylation methylation phosphorylation ubiquitination biotinylation and sumoylation chromatin remodeling and small RNA miRNA and siRNA directed DNA methyla- tion Wagner 2003 Vanyushin 2006 Fig. 1. These changes in gene expression could be fixed and passed into progeny transgenerational thus forming epigenetic memories. Various genes involved in epigenetic regulation of abiotic stress in plants are given in Table 1. sRNAs in response to abiotic stress Plants cope up with abiotic stress conditions by modifying certain biochemical pathways which change the physio- logicalprocessessuchasgrowthratefloweringtimeyield etc. The regulatory role of small RNAs has been well understood in the responses of plants to abiotic stress Sunkar et al. 2007 Ruiz-Ferrer and Voinnet 2009. Plants either up- or down regulate certain specific sRNAs or generatenewsRNAstotolerateabioticstressesKhraiwesh et al. 2012. The changing sRNA levels in response to different abiotic stresses were first observed in Arabidopsis Sunkar et al. 2005 which provided new insights for the investigation of plant stress signaling under abiotic stress conditions. With the development of high throughput sequencing technologies it has been possible to identify sRNAs Fahlgren et al. 2007 Xin et al. 2010 as well as several other categories of sRNAs involved in stress responses Ruiz-Ferrer and Voinnet 2009 Sunkar and Zhu 2007 Mallory 2006. Role of specific miRNAs in various abiotic stresses have been given in Table 2. sRNAs in response to drought Transcriptomics and proteomics analysis has contributed tremendously in identification of several genes regulated by altered expression of miRNAs in response to drought in numerous plant species like Arabidopsis cowpea soybean Triticum dicoccoides tobacco etc. miRNAs participate in the regulation of certain drought responsive genes and metabolites like dehydrins helicase proline RAB re- sponsive to abscisic acid vacuolar acid invertase glu- tathione S-transferase GST COR cold regulated abscisic acid ABA-inducible genes LEA late embryo- genesis abundant Rubisco etc. Nezhadahmadi et al. 2013. Recent studies have shown that in rice miR169 is a negative regulator of plant drought. It is down regulated to enhance the transcript levels of its target NFYA5 in existence of an abscisic acid responsive element ABRE under drought stresses Li et al. 2008 Zhao et al. 2009. Overexpression of miR169 causes plants to become hypersensitive to drought stress due to increased size of the stomatal aperture in leaves whereas over expression of NFYA5increasesplantresistancetodroughtduetosmaller stomatal aperture structures. Whereas over expression of miR396 miR394 miR164 miR408 and miR2118 enhan- ces drought resistance by changes in development or oxidative status related to target repression Song et al. 2013 Fang et al. 2014 Chen et al. 2015 Hajyzadeh et al. 2015 Wu et al. 2015. Extensive studies on plant model Arabidopsis have revealed that stress related miRNAs can be placed into three categories Jones-Rhoades and Bartel 2004 Liu et al. 2008 Sunkar and Zhu 2004. The first category includes miRNAs that target the transcription factors regulating the genes related to stress response in a plant e.g. miR156 miR159 miR165 miR169 miR171 miR172 miR319 etc. The second category comprised of miR167 that targets auxin response factors ARF6 and ARF8 Wu et al. 2011 miR168 targets ARGONAUTE1 AGO1 mRNA Vazquez et al. 2004 miR393 and miR394 that target F-box proteins Jain et al. 2007. Third category consists of miRNAs miR397 and miR408 which target hydrolase and oxidoreductase genes Apel and Hirt 2004 Kimura et al. 2003. It should be noted that the expression and drought response of miRNAs is species specific. For example miR166 is up regulated in Hordeum vulgare Kruszka et al. 2014 Triticum aestivum Akdogan et al. 2015 Pandey et al. 2014 and Saccharum spp. Bottino et al. 2013 Gentile et al. 2015 in response to drought whereas same was down regulated in Triticum dicoccoides Kantar et al. 2011 Populus euphratica Li Ind J Plant Physiol. October–December 2017 224:458–469 459 123 Authors personal copy

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et al. 2011a and Oryza sativa Zhou et al. 2010. At the molecular level many genes regulate mechanisms of drought stress tolerance. Many of them encode regulatory transcription factors such as members of AP2/ERF bZIP NAC HD-ZIP and MYB/MYC families which are important in regulating the expression of downstream genes Singh et al. 2002. sRNAs in response to heat and cold stress Plants often face suboptimal temperatures because of variations in geographical and seasonal conditions. sRNAs control the regulatory network related to plants’ response to temperature fluctuation. Heat-inducible miR156 helps in acquiring thermo tolerance. Over expression of miR156 enhances thermo tolerance Stief et al. 2014. Heat stress induces miR398 to repress CSD1 CDS2 and CCS. Fig. 1 Schematic representation of epigenetic mechanism of gene regulation in plants 460 Ind J Plant Physiol. October–December 2017 224:458–469 123 Authors personal copy

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Expression of a miR398-resistant form of CSD2 represses HSFs and HSPs thereby resulting in enhanced heat sen- sitivity Guan et al. 2013. Over expression of heat-re- pressible miR159 in rice decreases the expression of its target transcription factors TaGAMYB1 and TaGAMYB2 which directly affect starch metabolism causing hyper- sensitivity to heat Wang et al. 2012. Cold tolerance is regulated by miR165/166 miR319 miR393 miR396 miR402and miR408in Arabidopsis. miR156/157 miR159/ 319 miR164 miR394 and miR398 showed mild regula- tion under cold stress Sunkar and Zhu 2004 Liu et al. 2008. The C-repeat binding factor CBF cold-responsive pathway is the well-known cold tolerance pathway in plants Van Buskirk and Thomashow 2006. The CBF/ DREB1 family include three family members- CBF1 CBF2 and CBF3 DREB1b DREB1c and DREB1a respectively. These encode the DNA-binding proteins of Apetala2/ethylene responsive factor AP2/ERF family Gilmour et al. 1998. In Arabidopsis thaliana miR165/ 166 miR393 miR396 and miR408 were shown to be up regulated while miR156/157 miR159/319 miR164 miR394 and miR398 were observed to be either transient or mildly regulated under cold-stress Sunkar and Zhu 2004. sRNA in response to nutritional stress sRNAs also contribute to plant adaptation to nutritional stress for instance N P and S starvation through various mechanisms such as modulation of nitrogen uptake and transport the alteration of root architecture and production of metabolites and radical scavengers. miR167 miR393 and miR169 are involved in such regulations. During nitrogen availability miR167 is repressed while its target ARF6 is induced in the pericycle to initiate the lateral root that allow plants to search for N nutrients in the soil farther away from them Gifford et al. 2008. Table 1 Genes involved in epigenetic response to abiotic stress in plants and their roles Genes involved in plants epigenetic response Functions References Domains rearranged methyltransferase DRM CG CNG and CNN Contributes to de novo methylation of asymmetric sites Wada et al. 2003 and Cao and Jacobsen 2002a b Chromomethylase CMT Maintain CNG methylation in heterochromatin and silencing of methylated loci Bartee et al. 2001 Papa et al. 2001 and Tompa et al. 2002 Methyltransferase MET1 DNA methylation at CG sites post replicative de novo CpG methylation Finnegan and Kovac 2000 and Kankel et al. 2003 Methyl binding domain protein MBD Associated with histone and recognize methyl-cytosine Zemach and Grafi 2003 Histone deacetylase 19 HDA19 AtRPD3A Response to Jasmonic Acid and Ethylene Signaling induced by stress Zhou et al. 2005 DICER DICER-LIKE DCL 1 to 4 Cuts dsRNA into small fragments Schauer et al. 2002 RNA-denpendent RNA polymerase RDRM 1-6 Amplifies micro RNA Mourrain et al. 2000 and Vaistij et al. 2002 DEMETER DME/DNA glycosylase Demethylation of previously silenced sequences possibly in tissue-specific manner Morales-Ruiz et al. 2006 and Penterman et al. 2007 REPRESSOR OF SILENCING 1 ROS1/DNA glycosylase/lyase Demethylation activity on methylated but not demethylated DNA substrates Hypermethylation and transcriptional silencing of specific genes Agius et al. 2006 Penterman et al. 2007 and Zhu et al. 2007a b HISTONE DEACETYLASE 6 HDA6/histone deacetylase Reinforcing CpNpG methylation induced by RNA-directed transcriptional silencing Reactivation of previously silenced transgenes Local/repression Aufsatz et al. 2002 METHYL-CpG-BINDING DOMAIN PROTEINS AtMBDs 5-Methylcytosin binding proteins bind methylated CpG and induces local chromatin structure via modification of core histone proteins Zemach and Grafi 2007 LIKE HETEROCHROMATIN PROTEIN 1LHP1/ Binds to histone H3K9chromatin condensation Mylne et al. 2006 DECREASED DNA METHYLATION DDDDM1/SWI2/SNF2 DNA helicase Control of DNA methylation Zemach et al. 2005 Shaked et al. 2006 MA MAINETENANCE OF METHYLATION Transcription regulation of silent heterochromatic regions transgene silencing Vaillant et al. 2006 Ind J Plant Physiol. October–December 2017 224:458–469 461 123 Authors personal copy

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Table 2 Roles of specific miRNA in various abiotic stresses miRNA Plant species Abiotic stresses Target name References miR156 Wheat Heat stress SBP LIKE Khraiwesh et al. 2012 Maize Salt stress TSBP-domain protein 6 Sunkar and Zhu 2004 Ding et al. 2009 Lu et al. 2005 Jones-Rhoades and Bartel 2004 and Zhu et al. 2007a b A. thaliana T. dicoccoides H. vulgare O. sativa P. euphratica P. persica P. tomentosa S. bicolor Drought responsive SPL family of TFs Wu and Poethig 2006 Kantar et al. 2010 2011 Zhou et al. 2010 Li et al. 2011a Eldem et al. 2012 Ren et al. 2012 and Sanousi et al. 2016 miR157 Arabidopsis Hypoxia Stress Squamosa promoter Moldovan et al. 2010 P. persica Plant development SPL family of TFs Eldem et al. 2012 miR159 Wheat Heat stress MYB Khraiwesh et al. 2012 Rice Drought stress/Salt stress/Hypoxia stress TaGAMYB1 TaGAMYB2 Wang et al. 2012 Arabidopsis ABA stress MYB transcription factors UV-B stress Auxin responsive factor Sunkar and Zhou 2007 and Zhou 2007 ABA stress Auxin responsive factor A. thaliana O. sativa P. persica P. vulgaris Populus trichocarpa S. bicolor Drought responsive MYB and TCP TFs Reyes and Chua 2007 Zhou et al. 2010 Eldem et al. 2012 Arenas-Huertero et al. 2009 Shuai et al. 2013 and Sanousi et al. 2016 miR160 Wheat Heat stress ARF Khraiwesh et al. 2012 Maize Salt stress 40S ribosomal protein S16 P. persica P. tomentosa P. trichocarpa Drought responsive ARF 10 ARF 16 and ARF 17 Eldem et al. 2012 Ren et al. 2012 and Shuai et al. 2013 Barley Salinity ABA Bellutti et al. 2015 miR162 Maize Salt stress Endoribonuclease Dicer Cytochrome P450 Ding et al. 2009 and Lu et al. 2005 P. tomentosa Drought responsive DCL1 Ren et al. 2012 miR164 Maize Salt stress NAC domain protein NAC1 Lu et al. 2005 M. truncatula P. trichocarpa Drought responsive NAC TFs Wang et al. 2011 and Shuai et al. 2013 miR165/ 166 Arabidopsis UV-B stress HD-ZIP transcription factor Zhou 2007 P. persica Drought responsive HD-ZIPIII TFs Eldem et al. 2012 miR166 Maize Salt stress HD-ZIP Rolled leaf 1 Ding et al. 2009 Wheat Heat stress HD-ZIPIII Khraiwesh et al. 2012 T. dicoccoides G. max H. vulgare S. bicolor Drought responsive HD-ZIPIII TFs Kantar et al. 2010 2011 Li et al. 2011b and Sanousi et al. 2016 miR168 Arabidopsis Rice Maize Salt stress PZE40 protein Ding et al. 2009 Sunkar and Zhu 2004 and Lu et al. 2005 Wheat Heat stress AGO Khraiwesh et al. 2012 A. thaliana Z. mays O. Sativa P. persica miRNA biogenesis and mRna degradation AGO1 Liu et al. 2008 Zhou et al. 2010 Wei et al. 2009 and Eldem et al. 2012 miR169 Arabidopsis Rice Maize Drought stress CCAAT binding transcription factor Zhao et al. 2007 2009 and Zhou 2007 Salt stress Scarecrow-like Sunkar and Zhu 2004 Jones-Rhoades and Bartel 2004 and Zhou 2007 462 Ind J Plant Physiol. October–December 2017 224:458–469 123 Authors personal copy

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Table 2 continued miRNA Plant species Abiotic stresses Target name References Rice Salt stress CCAAT- box binding transcription factor carrying NF-YA gene Wheat Heat stress MtHAP2-1 Khraiwesh et al. 2012 Tomato O. Sativa P. persica G. max M. truncatula P. tomentosa Rapeseed Plant development and response to different abiotic stresses CBF TFs Zhang et al. 2011 Zhao et al. 2007 2010 Wang et al. 2011 Trindade et al. 2010 Eldem et al. 2012 Li et al. 2011b Ren et al. 2012 and Jian et al. 2016 miR170/ 171 Arabidopsis Rice Salt stress Transcription factors Sunkar and Zhu 2004 Jones-Rhoades and Bartel 2004 Zhou 2007 and Moldovan et al. 2010 Maize Salt stress Sprouty homologue 2Spry-2 Arabidopsis Cold stress Transcription factor GAMyb Zhang et al. 2008a Rice Drought responsive MYB family miR170 O. sativa Radial patterning in roots and floral development SCL-TFs Zhou et al. 2010 miR172 Arabidopsis UV-B stress drought stress Hypoxia stress AP2 Bziptf MYB Sunkar and Zhu 2004 Jones-Rhoades and Bartel 2004 Zhou 2007 and Moldovan et al. 2010 Maize Salt stress Transcription factor GAMyb Zhang et al. 2008b Wheat Drought responsive Protein kinase Zhang et al. 2008a b O. sativa P. tomentosa Heat responsive TIR1 F box proteins Zhao et al. 2007 and Zhou 2007 miR390 P. tomentosa P. persica Auxin mediated transcriptional activation ARF Ren et al. 2012 and Eldem et al. 2012 miR391 Arabidopsis Hypoxia Protein kinase Zhang et al. 2008a miR393 A. thaliana P. persica P. vulgaris S. bicolor Susceptibility to virulent bacteria T1R1 AFB2 and AFB3 Liu et al. 2008 Eldem et al. 2012 Arenas- Huerteroetal.2009andSanousietal.2016 ABA salt stress Kepinski and Leyser 2005 Heat stress T1R1 Khraiwesh et al. 2012 Wheat Heat stress Zhou et al. 2010 Eldem et al. 2012 and Ren et al. 2012 miR394 P. tomentosa P. trichocarpa G. max Abiotic stress response Dehydration responsive protein F-box proteins Renetal.2012Shuaietal.2013andLietal. 2011b miR395 Maize Salt stress ATP sulfurylase Zhang et al. 2008b O. sativa P. persica P. tomentosa Response to sulphate deprivation ATP sulfurylase Zhou et al. 2010 Wang et al. 2011 Eldem et al. 2012 miR396 Maize Salt stress Laccases A. thaliana O. sativa M. truncatula P. persica Salt stress GRL TFs ceramidasegenes Liu et al. 2008 Zhou et al. 2010 Wang et al. 2011 and Eldem et al. 2012 miR397 Arabidopsis Rice Salt stress Laccases Sunkar and Zhu 2004 and Zhu et al. 2007a b Cold stress Casein Kinase II A. thaliana O. sativa M. truncatula P. persica Laccases Lignin biosynthesis and stress response Sunkar and Zhu 2004 Zhou et al. 2010 Eldem et al. 2012 and Ren et al. 2012 miR398 M. truncatula T. dicoccoides P. persica Oxidative stress CuSOD Cytochrome C oxidase subunit V Trindade et al. 2010 Wang et al. 2011 Kantar et al. 2011 and Eldem et al. 2012 Ind J Plant Physiol. October–December 2017 224:458–469 463 123 Authors personal copy

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In addition miR826 and miR5090 regulate N metabo- lism He et al. 2014. These miRNAs target the 2-oxog- lutarate dependent dioxygenase Alkenyl Hydroxalkyl Producing 2 AOP2 involved in the synthesis of glucosi- nolates He et al. 2014. The reduced glucosinolate con- tents enable the distribution of N to other nitrogen- containing metabolites important for plant growth and development which in turn increase plant resistance to N deprivation. Another well-characterized miRNAs in angiosperms is miR399 Sunkar and Zhu 2004 Valdes- Lopez et al. 2008 Hu et al. 2011 that control phosphate Pi uptake and homeostasis. This miR399 targets PHO2 which encodes an ubiquitin-conjugating E2 enzyme regu- lator of Pi uptake translocation and remobilization under Pi-sufficient conditions Sunkar and Zhu 2004 Fujii et al. 2005 Bari et al. 2006 Chiou et al. 2006. Under P limiting conditions miR399 is up regulated in shoot and then relocated to root where it suppresses PHO2 allowing the translocation of Pi from root to shoot Pant et al. 2008. This suggests that miR399 serves as a mobile signal to modulate Pi uptake and translocation from root to shoot Pant et al. 2008. Sulfur is another macronutrient neces- sary for plant growth and development. Sulfur deficiency induces the expression of miR395 via SULPHUR LIM- ITATION 1 SLIM1 an ETHYLENE-INSENSITIVE- LIKE EIL family transcription factor Jones-Rhoades and Bartel 2004 Kawashima et al. 2009 2011 Liang et al. 2010. miR395 targets ATP sulphurylases APS1 APS3 and APS4 and the high affinity sulfate transporter 2 Kawashima et al. 2009 Liang et al. 2010 Kawashima et al. 2011. The induction of miR395 by sulfur limitation down regulates APS1 APS4 and shoot SULTR21 but not root SULTR21 and APS3 because their expression domains are spatially different from those of miR395 Table 2 continued miRNA Plant species Abiotic stresses Target name References Rice UV-B stress Cytochrome C oxidase Subunit V Arabidopsis Copper Superoxide dismutase1 CSD1 Yamasaki 2007 miR399 Arabidopsis Salt stress Hasty Rice Granule-bound starch synthase M. truncatula P. tomentosa Phosphate starvation Unknown targets Wang et al. 2011 and Ren et al. 2012 miR401 Arabidopsis UV-B stress Unknown proteins Zhou 2007 miR403 P. tomentosa Rapeseed miRNA functioning AGO2 Ren et al. 2012 and Jian et al. 2016 miR408 Arabidopsis Drought stress Peptide chain release factor plantacyanin Lu et al. 2005 miR417 Arabidopsis ABA drought salt stress Unknown targets Jung and Kang 2007 miR472 P. tomentosa P. trichocarpa CC-NBS-LRR domain Ren et al. 2012 and Shuai et al. 2013 miR473 P. tomentosa P. trichocarpa Signal transduction and development GRAS TFs Ren et al. 2012 and Shuai et al. 2013 miR474 Populus Maize Salt stress Pumilio/Mpt5 family Zhang et al. 2008a b O. sativa T. dicoccoides Z. mays Kinesin a PPR family protein Organelle biogenesis Zhou et al. 2010 Kantar et al. 2011 and Wei et al. 2009 miR475 P. tomentosa RNA editing PPR protein Ren et al. 2012 miR482 P. tomentosa G. max Cellular metabolism Cyt P450 Ren et al. 2012 and Li et al. 2011b miR528 Z. mays Elimination of ROS POD Wei et al. 2009 miR529 O. sativa Hypoxia stress AP2 like TFs SPL TFs Zhou et al. 2010 miR775 Arabidopsis Hypoxia stress Galactosyltransferase family Moldovan et al. 2010 miR824 Rapeseed Regulation of flowering time MADS box TFs Jian et al. 2016 miR827 Wheat Heat stress Unknown Khraiwesh et al. 2012 464 Ind J Plant Physiol. October–December 2017 224:458–469 123 Authors personal copy

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Kawashima et al. 2011. Consequently the translocation of sulfur from root to shoot is enhanced whereas the transportation from shoot to root is reduced Kawashima et al. 2011. Thus miR395 regulates sulfur homeostasis through spatial restriction of APS expression Kawashima et al. 2011. sRNAs involved in salinity stress Salt stress is induced by accumulation of large amount of salts delivered along with irrigation water and through high evapotranspiration rates caused by climatic changes. It has been predicted that the by 2050 50 of world arable land will be affected by salt. Several genes and pathways in plants are affected by salt stress. Besides genes numerous differentially regulated miRNAs have also been identified in salt-stressed plants. miRNAs often regulate plant resis- tance or tolerance to salinity stress by modulating the hormone-signaling pathways. Among these miR158 miR159 miR165 miR167 miR168 miR169 miR171 miR319 miR393 miR394 miR396 and miR397 have been reported to be over expressed in response to salt whereas miR398 is down regulated Liu et al. 2008. Overexpression of salinity-inducible miR393 reduces the levels of TIR1 and AFB2 and causes hypersensitivity to salinity stress whereas expression of a miR393-resistant TIR1 transgene increases plant tolerance to salinity Chen et al. 2011 Iglesias et al. 2014. Another example is miR394. Plants with elevated levels of miR394 display hypersensitivity to salinity stress in an ABA-dependent manner whereas plants harboring a miR394-resistant LCR have increased salinity and ABA tolerance Song et al. 2013. Two salinity inducible miRNAs miR319 and miR528 can positively affect plant response to salinity stress through the down regulation of their targets Zhou et al. 2013 Yuan et al. 2015. Role of miRNA in oxidative response Reactive oxygen is innate to plants because it has been produced persistently by aerobic processes Mittler et al. 2004. However the excessive production of reactive oxy- gen species causes Oxidative stress. Reactive oxygen spe- cies contains super-oxide radicals O 2 - hydrogen peroxide H 2 O 2 and hydroxyl radicals OH - produced by various environmental stresses such as drought stress heavymetalsnutrientdeprivationandsaltstressitleadsto extreme oxidative damage to nucleic acids proteins and membrane lipids. Plants have derived specialized mecha- nisms of reducing the harmful effects of ROS. Enzymes such as superoxide dismutases SODs catalases and peroxidases has been involved in enzymatic mechanism whereas many plant based compounds such as carotenoids xanthophylls glutathione tocopherol ascorbate etc. has been involved in non-enzymatic mechanism. Based on the metal cofactor study SODs have been categorized into three parts: iron SOD FeSOD manganese SOD MnSOD and Copper–zinc SOD Cu/ZnSOD Mittler 2002. miR398 in Arabidopsis has been reported to target the transcript of Cu/Zn-SODs CSD1 cytosolic and CSD2 chloroplastic Jagadeeswaran et al. 2009. The study of microRNA interactions upon biotic and abiotic stress is of great importance in association with the expression change in the miR398 level. Conclusion The changing climate and variable weather patterns are a matter of major concern for agricultural crop production. Various abiotic stresses act as a limiting factor in crop production and yield across the world. Extensive research has beencarriedoutdepicting thecontribution ofsRNAsin plant abiotic stress tolerance. These researches have demonstrated the pivotal roles of sRNAs in the gene reg- ulation mechanism during different stress conditions. Studies in plant miRNAs have identified a large number of conserved and non-conserved miRNAs in response to abiotic stress along with their differential expression pat- terns in plants. High throughput sequencing technologies like transcriptome sequencing degradome sequencing and computational approaches have been instrumental in gen- ome-wide miRNA expression profiling with respect to abiotic stresses. Research of epigenetic regulation in response to abiotic stress has been accomplished in the last several years especially in the model plant Arabidopsis. Changes in histone modifications and changes in the expression of genes encoding histone modifying enzymes as well as changes in DNA methylation patterns and the effect ofsmall RNAshave beenshown toplaycriticalroles in the response to abiotic stress at a gene-specific and genome-wide level. The completion of the plant genomes rice maize and Brachypodium as well as the rapid pro- gress inthe sequencingof wheatand barley will contribute significantly to this endeavor and enable the generation of improved varieties with increased stress. Acknowledgements We are highly thankful to the Director of our Institute for providing all kind of assistance and also thankful to ICAR for providing grants support in the form of Lal Bahadur Shashtri Award. Ind J Plant Physiol. October–December 2017 224:458–469 465 123 Authors personal copy

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