sRNA and epigenetic

Views:
 
     
 

Presentation Description

sRNA and epigenetic mediated abiotic stress tolerance in plants:

Comments

Presentation Transcript

slide 1:

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

slide 2:

123 Your article is protected by copyright and all rights are held exclusively by Indian Society for Plant Physiology. This e-offprint is for personal use only and shall not be self- archived in electronic repositories. If you wish to self-archive your article please use the accepted manuscript version for posting on your own website. You may further deposit the accepted manuscript version in any repository provided it is only made publicly available 12 months after official publication or later and provided acknowledgement is given to the original source of publication and a link is inserted to the published article on Springers website. The link must be accompanied by the following text: "The final publication is available at link.springer.com”.

slide 3:

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 Pradeep.sharmaicar.gov.in 1 ICAR-IndianInstituteofWheat andBarleyResearch Karnal India 123 Ind J Plant Physiol. October–December 2017 224:458–469 https://doi.org/10.1007/s40502-017-0330-z Authors personal copy

slide 4:

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

slide 5:

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

slide 6:

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

slide 7:

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

slide 8:

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

slide 9:

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

slide 10:

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

slide 11:

References Agius F. Kapoor A. Zhu J. K. 2006. Role of the arabidopsis DNA glycosylase/lyase ROS1 in active DNA demethylation. Proceedings of the National Academy of Sciences 103 11796–11801. Akdogan G. Tufekci E. D. Uranbey S. Unver T. 2015. miRNA-based drought regulation in wheat. Functional Integrative Genomics 16 221–233. Ambros V. 2004. The functions of animal microRNAs. Nature 431 350–355. Apel K. Hirt H. 2004. Reactive oxygen species: Metabolism oxidative stress and signal transduction. Annual Review of Plant Biology 55 373–399. Arenas-Huertero C. Perez B. Rabanal F. Blanco-Melo D. De la Rosa C. Estrada-Navarrete G. et al. 2009. Conserved and novel miRNAs in the legume Phaseolus vulgaris in response to stress. Plant Molecular Biology 70 385–401. Aufsatz W. Mette M. F. van der Winden J. Matzke M. Matzke A. J. M. 2002. HDA6 a putative histone deacetylase needed to enhance DNA methylation induced by double- stranded RNA. The EMBO Journal 21 6832–6841. Bari R. Datt Pant B. Stitt M. Scheible W. R. 2006. PHO2 microRNA399 and PHR1 define a phosphate-signaling pathway in plants. Plant Physiology 141 988–999. Bartee L. Malagnac F. Bender J. 2001. Arabidopsis cmt3 chromomethylase mutations block non-CG methylation and silencing of an endogenous gene. Genes Development 15 1753–1758. Bartel D. P. 2004. Micro RNAs: Genomics biogenesis mechanism and function. Cell 116 281–297. Baulcombe D. 2004. RNA silencing in plants. Nature 431 356–363. Bellutti F. Kauer M. Kneidinger D. Lion T. Klein R. 2015. Identification of RISC-associated adenoviral microRNAs a subset oftheir direct targets and global changes inthe targetome upon lytic adenovirus 5 infection. Journal of Virology 893 1608–1627. Borsani O. Zhu J. Verslues P. E. Sunkar R. Zhu J. K. 2005. Endogenous siRNAs derived from a pair of natural cis-antisense transcripts regulate salt tolerance in Arabidopsis. Cell 1237 1279–1291. Bottino M. C. Rosario S. Grativol C. Thiebaut F. Rojas C. A. Farrineli L. et al. 2013. High-throughput sequencing of small RNA transcriptome reveals salt stress regulated microRNAs in sugarcane. PLoS One 8 e59423. https://doi.org/10.1371/journal. pone.0059423. Budak H. Kantar M. Bulut R. Akpinar B. A. 2015. Stress responsive miRNAs and isomiRs in cereals. Plant science 235 1–13. Cao X. Jacobsen S. 2002a. Locus-specific control of asymmet- ric and CpNpG methylation by the DRN and CMT3 methyl- transferase genes. Proceedings of National Academy of Sciences 4 16491–16498. Cao X. Jacobsen S. E. 2002b. Role of the Arabidopsis DRM methyltransferases in de novo DNA methylation and gene silencing. Current Biology 12 1138–1144. Carthew R. W. Sontheimer E. J. 2009. Origins and mechanisms of miRNAs and siRNAs. Cell 136 642–655. Chen Z. H. Bao M. L. Sun Y. Z. Yang Y. J. Xu X. H. Wang J. H. et al. 2011. Regulation of auxin response by miR393- targeted transport inhibitor response protein 1 is involved in normal development in Arabidopsis. Plant Molecular Biology 77 619–629. ChenL.LuanY.ZhaiJ.2015.Sp-miR396a-5pacts asastress- responsive genes regulator by conferring tolerance to abiotic stresses and susceptibility to Phytophthora nicotianae infection in transgenic tobacco. Plant Cell Reports 34 2013–2025. ChiouT.J.AungK.LinS.I.WuC.C.ChiangS.F.SuC.L. 2006. Regulation of phosphate homeostasis by microRNA in Arabidopsis. Plant Cell 18 412–421. Ding D. Zhang L. Wang H. Liu Z. Zhang Z. Zheng Y. 2009. Differential expression of miRNAs in response to salt stress in maize roots. Annals of Botany 1031 29–38. Eldem V. Akcay U. C. Ozhuner E. Bakir Y. Uranbey S. Unver T. 2012. Genome-wide identification of miRNAs responsive to drought in peach Prunus persica by high- throughput deep sequencing. PLoS One 712 e50298. Fahlgren N. Howell M. D. Kasschau K. D. 2007. High throughput sequencing of Arabidopsis microRNAs: Evidence for frequent birth and death of MIRNA genes. PLoS ONE 2 e219. Fang Y. Xie K. Xiong L. 2014. Conserved miR164-targeted NAC genes negatively regulate drought resistance in rice. Journal of Experimental Botany 65 2119–2135. Finnegan E. J. Kovac K. A. 2000. Plant DNA methyltrans- ferases. Plant Molecular Biology 432–3 189–201. Finnegan E. J. Matzke M. A. 2003. The small RNA world. Journal of Cell Science 116 4689–4693. Fujii H. Chiou T. J. Lin S. I. Aung K. Zhu J. K. 2005. A miRNA involved in phosphate-starvation response in Arabidop- sis. Current Biology 15 2038–2043. Gentile A. Dias L. I. Mattos R. S. Ferreira T. H. Menossi M. 2015. MicroRNAs and drought responses in sugarcane. Fron- tiers in Plant Science 6 58. Gifford M. L. Dean A. Gutierrez R. A. Coruzzi G. M. Birnbaum K. D. 2008. Cell specific nitrogen responses mediated developmental plasticity. Proceedings of the National Academy of Sciences 105 803–808. Gilmour S. J. Zarka D. G. Stockinger E. J. Salazar M. P. Houghton J. M. Thomashow M. F. 1998. Low temperature regulation of the Arabidopsis CBF family of AP2 transcriptional activators as an early step in cold-induced COR gene expression. Plant Journal 164 433–442. Gottesman S. 2005. Micros for microbes: Non-coding regulatory RNAs in bacteria. Trends in Genetics 21 399–404. Guan Q. Lu X. Zeng H. Zhang Y. Zhu J. 2013. Heat stress induction of miR398 triggers a regulatory loop that is critical for thermotolerance in Arabidopsis. Plant Journal 74 840–851. Hajyzadeh M. Turktas M. Khawar K. M. Unver T. 2015. miR408 overexpression causes increased drought tolerance in chickpea. Gene 555 186–193. He H. Liang G. Li Y. Wang F. Yu D. 2014. Two young MicroRNAs originating from target duplication mediatenitrogen starvation adaptation via regulation of glucosinolate synthesis in Arabidopsis thaliana. Plant Physiology 164 853–865. Hu B. Zhu C. Li F. Tang J. Wang Y. Lin A. et al. 2011. LEAF TIP NECROSIS1 plays a pivotal role in the regulation of multiple phosphate starvation responses in rice. Plant Physiol- ogy 156 1101–1115. Iglesias M. J. Terrile M. C. Windels D. Lombardo M. C. Bartoli C. G. Vazquez F. et al. 2014. MiR393 regulation of auxin signaling and redox-related components during acclimation to salinity in Arabidopsis. PLoS ONE 9 e107678. Jagadeeswaran G. Saini A. Sunkar R. 2009. Biotic and abiotic stress down-regulate miR398 expression in Arabidopsis. Planta 2294 1009–1014. Jain M. Nijhawan A. Arora R. Agarwal P. Ray S. Sharma P. et al. 2007. F-box proteins in rice. Genome-wide analysis classification temporal and spatial gene expression during 466 Ind J Plant Physiol. October–December 2017 224:458–469 123 Authors personal copy

slide 12:

panicle and seed development and regulation by light and abiotic stress. Plant Physiology 143 1467–1483. Jian H. Wang J. Wang T. Wei L. Li J. Liu L. 2016. Identification of rapeseed microRNAs involved in early stage seed germination under salt and drought stresses. Frontiers in Plant Science 7 658. Jones-Rhoades M. W. Bartel D. P. 2004. Computational identification of plant microRNAs and their targets including a stress-induced miRNA. Molecular Cell 14 787–799. Jung H. J. Kang H. 2007. Expression and functional analysis of microRNA417 in Arabidopsis thaliana under stress conditions. Plant Physiology and Biochemistry 45 805–811. Kamthan A. Chaudhuri A. Kamthan M. Datta A. 2015. Small RNAs in plants: Recent development and application for crop improvement. Frontiers in plant science 6 208. Kankel M. W. Ramsey D. E. Stokes T. L. Flowers S. K. Haag J. R. Jeddeloh J. A. et al. 2003. Arabidopsis MET1 cytosine methyltransferase mutants. Genetics 163 1109–1122. Kantar M. Lucas S. Budak H. 2011. miRNA expression patterns of Triticum dicoccoides in response to shock drought stress. Planta 233 471–484. Kantar M. Unver T. Budak H. 2010. Regulation of barley miRNAs upon dehydration stress correlated with target gene expression. Functional Integrative Genomics 104 493–507. Kawashima C. G. Matthewman C. A. Huang S. Q. Lee B. R. Yoshimoto N. Koprivova A. et al. 2011. Interplay of SLIM1 and miR395 in the regulation of sulfate assimilation in Ara- bidopsis. Journal of Plant 66 863–876. Kawashima C. G. Yoshimoto N. Maruyama-Nakashita A. Tsuchiya Y. N. Saito K. Takahashi H. et al. 2009. Sulphur starvation induces the expression of microRNA-395 and one of its target genes but in different cell types. Plant Journal 57 313–321. Kepinski S. Leyser O. 2005. The Arabidopsis F-box protein TIR1 is an auxin receptor. Nature 4357041 446–451. Khraiwesh B. Zhu J. K. Zhu J. 2012. Role of miRNAs and siRNAs in biotic and abiotic stress responses of plant. Biochim- ica et Biophysica Acta 1819 137–148. Kimura M. Manabe K. Abe T. Yoshida S. Matsui M. Yamamoto Y. Y. 2003. Analysis of hydrogen peroxide- independent expression of the high-light-inducible ELIP2 gene with the aid of the ELIP2 promoter–luciferase fusions. Journal of Photochemistry and Photobiology 77 668–674. Kruszka K. Pacak A. Swida-Barteczka A. Nuc P. Alaba S. Wroblewska Z. et al. 2014. Transcriptionally and posttran- scriptionally regulated micro RNAs in heat stress response in barley. Journal of Experimental Botany 65 6123–6135. Li H. Dong Y. Yin H. Wang N. Yang J. Liu X. et al. 2011a. Characterization of the stress associated microRNAs in Glycine max by deep sequencing. BMC Plant Biology 11 170. 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. Plant Cell 20 2238–2251. Li B. Qin Y. Duan H. Yin W. Xia X. 2011b. Genome-wide characterization of new and drought stress responsive micro- RNAs in Populus euphratica. Journal of Experimental Botany 62 3765–3779. Liang G. Yang F. Yu D. 2010. MicroRNA395 mediates regulation of sulfate accumulation and allocation in Arabidopsis thaliana. Plant Journal 62 1046–1057. Liu H. H. Tian X. Li Y. J. Wu C. A. Zheng C. C. 2008. Microarray-based analysis of stress-regulated microRNAs in Arabidopsis thaliana. RNA 14 836–843. Lu S. Sun Y. H. Shi R. Clark C. Li L. Chiang V. L. 2005. Novel and mechanical stress-responsive microRNAs in Populus trichocarpa that are absent from Arabidopsis. Plant Cell 17 2186–2203. Mallory Vaucheret. 2006. Functions of plant microRNAs and related small RNAs. Nature Genetics 38 S31–S33. Mallory A. C. Dugas D. V. Bartel D. P. Bartel B. 2004. MicroRNA regulation of NAC-domain targets is required for proper formation and separation of adjacent embryonic vege- tative and floral organs. Current Biology 14 1035–1046. Mittler R. 2002. Oxidative stress antioxidants and stress tolerance. Trends in Plant Sciences 79 405–410. Mittler R. Vanderauwera S. Gollery M. Van Breusegem F. 2004. Reactive oxygen gene network of plants. Trends in Plant Sciences 9 490–498. Moldovan D. Spriggs A. Yang J. Pogson B. J. Dennis E. S. Wilson I.W.2010. Hypoxia responsive microRNAs andtrans- acting small interfering RNAs in Arabidopsis. Journal of Experimental Botany 611 165–177. Morales-Ruiz T. Ortega-Galisteo A. P. Ponferrada-Marin M. I. MartinezMacias M. I. Ariza R. R. Roldan-Arjona T. 2006. Demeter and Repressor of scilncing 1 encode 5-methyl- cytosine DNA glycosylases. Proceedings of National Academy of Science 103 6853–6858. Morita T. Mochizuki Y. Aiba H. 2006. Translational repression is sufficient for gene silencing by bacterial small noncoding RNAs in the absence of mRNA destruction. Pro- ceedings of the National Academy of Sciences 103 4858–4863. Mourrain P. Be ´clin C. Elmayan T. Feuerbach F. Godon C. Morel J. B. et al. 2000. Arabidopsis SGS2 and SGS3 genes are required for posttranscriptional gene silencing and natural virus resistance. Cell 1015 533–542. Mylne J. S. Barrett L. Tessadori F. Mesnage S. Johnson L. Bernatavichute Y. V. et al. 2006. LHP1 the Arabidopsis homologue of HETEROCHROMATIN PROTEIN1 is required for epigenetic silencing of FLC. Proceedings of the National Academy of Sciences 103 5012–5017. Nezhadahmadi A. Prodhan Z. H. Faruq G. 2013. Drought tolerance in wheat. Scientific World Journal. https://doi.org/10. 1155/2013/610721. Pandey R. Joshi G. Bhardwaj A. R. Agarwal M. Katiyar- Agarwal S. 2014. A comprehensive genome-wide study on tissue-specific and abiotic stress-specific miRNAs in Triticum aestivum. PLoS ONE 9 e95800. https://doi.org/10.1371/journal. pone.0095800. Pant B. D. Buhtz A. Kehr J. Scheible W. R. 2008. MicroRNA399 is a long-distance signal for the regulation of plant phosphate homeostasis. Plant Journal 53 731–738. Papa C. M. Springer N. M. Muszynski M. G. Meeley R. Kaeppler S. M. 2001. Maize chromomethylase Zea methyl- transferase2 is required for CpNpG methylation. Plant Cell 138 1919–1928. Penterman J. Zilberman D. Huh J. H. Ballinger T. Henikoff S. Fischer R. L. 2007. DNA demethylation in the Arabidopsis genome. Proceedings of the National Academy of Sciences 104 6752–6757. Ren Y. Chen L. Zhang Y. Kang X. Zhang Z. Wang Y. 2012. Identification of novel and conserved Populus tomentosa microRNA as components of a response to water stress. Functional Integrative Genomics 12 327–339. Reyes J. L. Chua N. H. 2007. ABA induction of miR159 controls transcript levels oftwo MYBfactors duringArabidopsis seed germination. Plant Journal 49 592–606. Rodriguez M. Canales E. Borras Hidalgo O. 2005. Molecular aspects of abiotic stress in plants. Biotecnolgia Aplicada 22 1–10. Ind J Plant Physiol. October–December 2017 224:458–469 467 123 Authors personal copy

slide 13:

Ruiz-Ferrer V. Voinnet O. 2009. Roles of plant small RNAs in biotic stress responses. Annual Review of Plant Biology 60 485–510. SanousiR.S.E.HamzaN.B.AbdelmulaA.A.MohammedI.A. Gasim S. M. Mishra N. 2016. Differential expression of miRNAs in Sorghum bicolor under drought and salt stress. American Journal of Plant Sciences 7 870–878. Schauer S. E. Jacobsen S. E. Meinke D. W. Ray A. 2002. DICER-LIKE1: Blind men and elephantsn in Arabidopsis de- velopment. Trends in Plant Sciences 711 487–491. Shaked H. Avivi-Ragolsky N. Levy A. A. 2006. Involvement of the Arabidopsis SWI2/SNF2 chromatin remodeling gene family in DNA damage response and recombination. Genetics 173 985–994. Shuai P. Liang D. Zhang Z. Yin W. Xia X. 2013. Identification of drought-responsive and novel Populus tri- chocarpa microRNAs by high-throughput sequencing and their targets using degradome analysis. BMC Genomics 14 233. Singh K. B.Foley R. C. Onate-Sanchez L.2002. Transcription factors in plant defense and stress responses. Current Opinion in Plant Biology 5 430–436. Song J. B. Gao S. Sun D. Li H. Shu X. X. Yang Z. M. 2013. miR394 and LCR are involved in Arabidopsis salt and drought stress responses in an abscisic acid-dependent manner. BMC Plant Biology 13 210. Stief A. Altmann S. Hoffmann K. Pant B. D. Scheible W. R. Baurle I. 2014. Arabidopsis miR156 regulates tolerance to recurring environmental stress through SPL transcription factors. Plant Cell 26 1792–1807. Sunkar R. Chinnusamy V. Zhu J. H. Zhu J. K. 2007. Small RNAsasbigplayersinplantabioticstress responsesandnutrient deprivation. Trends in Plant Science 12 301–309. Sunkar R. Girke T. Zhu J. K. 2005. Identification and characterization of endogenous small interfering RNAs from rice. Nucleic Acids Research 33 4443–4454. Sunkar R. Zhu J. K. 2004. Novel and stress-regulated microRNAs and other small RNAs from Arabidopsis. Plant Cell 168 2001–2019. Sunkar R. Zhu J. K. 2007. Micro RNAs and Short interfering RNAs in plants. Journal of Integrative Plant Biology 49 817–826. Tompa R. McCallum C. M. Delrow J. Henikoff J. G. Van Steensel B. Henikoff S. 2002. Genome-wide profiling of DNA methylation reveals transposon targets of CHROMO- METHYLASES3. Current Biology 12 65–68. Trindade I. Capitao C. Dalmay T. Fevereiro M. P. Santos D. M. 2010. miR398 and miR408 are upregulated in response to water deficit in Medicago truncatula. Planta 2313 705–716. Vaistij F. E. Jones L. Baulcombe D. C. 2002. Spreading of RNA targeting and DNA methylation in RNA silencing requires transcription of the target gene and a putative RNA-dependent RNA polymerase. Plant Cell 144 857–867. Valdes-Lopez O. Arenas-Huertero C. Ramirez M. Girard L. Sanchez F. Vance C. P. et al. 2008. Essential role of MYB transcription factor: PvPHR1 and microRNA: PvmiR399 in phosphorus-deficiency signalling in common bean roots. Plant Cell and Environment 31 1834–1843. Vaillant I. Schubert I. Tourmente S. Mathieu O. 2006. MOM1 mediates DNA-methylation-independent silencing of repetitive sequences in Arabidopsis. EMBO Reports 712 1273–1278. https://doi.org/10.1038/sj.embor.7400791. Van Buskirk H. A. Thomashow M. F. 2006. Arabidopsis transcription factors regulating cold acclimation. Physiologia Plantarum 1261 72–80. Vanyushin B. F. 2006. DNA methylation in plants. Current Topics in Microbiology and Immunology 301 67–122. Vazquez F. 2006. Arabidopsis endogenous small RNAs: Highways and byways. Trends in Plant Science 119 460–468. Vazquez F. Gasciolli V. Crete P. Vaucheret H. 2004. The nuclear dsRNA binding protein HYL1 is required for microRNA accumulation and plant development but not posttranscriptional transgene silencing. Current Biology 14 346–351. Wada Y.Ohya H.Yamaguchi Y.KoizumiN. SanoH.2003. Preferential de novomethylation of cytosine residues in non- CpG sequencesby a domains rearranged DNA methyltransferase from tobacco plants. Journal of Biological Chemistry 27843 42386–42393. Wagner D. 2003. Chromatin regulation of plant development. Current Opinion in Plant Biology 6 20–28. Wang T. Chen L. Zhao M. Tian Q. Zhang W. H. 2011. Identification of drought-responsive microRNAs in Medicago truncatula by genome-wide high-throughput sequencing. BMC Genomics 12 367. Wang Y. Sun F. Cao H. Peng H. Ni Z. Sun Q. et al. 2012. TamiR159 directed wheat TaGAMYB cleavage and its involve- ment in anther development and heat response. PLoS ONE 7 e48445. Wei L. Zhang D. Xiang F. Zhang Z. 2009. Differentially expressed miRNAs potentially involved in the regulation of defense mechanism to drought stress in maize seedlings. International Journal of Plant Sciences 1708 979–989. Whitelaw N. C. Whitelaw E. 2006. How lifetimes shape epigenotype within and across generations. Human Molecular Genetics 152 131–137. Wu B. F. Li W. F. Xu H. Y. Qi L. W. Han S. Y. 2015. Role of cinmiR2118 in drought stress responses in Caragana inter- media and Tobacco. Gene 574 34–40. Wu G. Poethig R. S. 2006. Temporal regulation of shoot development in Arabidopsis thaliana by miR156 and its target SPL3. Development 133 3539–3547. Wu Y. Wei B. Liu H. Li T. Rayner S. 2011. MiRPara: A SVM-based software tool for prediction of most probable microRNA coding regions in genome scale sequences. BMC Bioinformatics 12 107. Xin M. M. Wang Y. Yao Y. Y. Xie C. J. Peng H. R. Ni Z. F. et al. 2010. Diverse set of microRNAs are responsive to powdery mildew infection and heat stress in wheat Triticumaes- tivum L.. BMC Plant Biology 10 123. Yamasaki H. 2007. Regulation of copper homeostasis by micro- RNA in Arabidopsis. Journal of Biological Chemistry 282 16369–16378. Yuan S. Li Z. Li D. Yuan N. Hu Q. Luo H. 2015. Constitutive expression of rice microRNA528 alters plant development and enhances tolerance to salinity stress and nitrogen starvation in creeping bentgrass. Plant Physiology 169 576–593. Zemach A. Grafi G. 2003. Characterization of Arabidopsis thaliana methyl-CpG-binding domain MBD proteins. Plant Journal 345 565–572. Zemach A. Grafi G. 2007. Methyl-CpG-binding domain proteins in plants: Interpreters of DNA methylation. Trends in Plant Science 12 80–85. Zemach A. Li Y. Wayburn B. Ben-Meir H. Kiss V. Avivi Y. et al. 2005. DDM1 binds Arabidopsis methyl-CpG binding domain proteins and affects their subnuclear localization. Plant Cell 17 1549–1558. Zhang Z. X. Wei L. Y. Zou X. L. Tao Y. S. Liu Z. J. Zheng Y. L. 2008a. Submergence-responsive microRNAs are poten- tially involved in the regulation of morphological and metabolic adaptations in maize root cells. Annals of Botany 102 509–519. Zhang X. Wollenweber B. Jiang D. Liu F. Zhao J. 2008b. Water deficits and heat shock effects on photosynthesis of a 468 Ind J Plant Physiol. October–December 2017 224:458–469 123 Authors personal copy

slide 14:

transgenic Arabidopsis thaliana constitutively expressing ABP9 a bZIP transcription factor. Journal of Experimental Botany 59 839–848. Zhang X. Zhao H. Gao S. Wang W. C. Katiyar-Agarwal S. Huang H. D. et al. 2011. Arabidopsis argonaute 2 regulates innate immunity via miRNA393-mediated silencing of a golgi- localized SNARE Gene MEMB12. Molecular Cell 423 356–366. Zhao B. Ge L. Liang R. Li W. Ruan K. Lin H. et al. 2009. Members of miR-169 family are induced by high salinity and transiently inhibit the NF-YA transcription factor. BMC Mol. Biology 10 29. Zhao B. Liang R. Ge L. Li W. Xiao H. Lin H. et al. 2007. Identification of drought-induced microRNAs in rice. Biochem- ical and Biophysical Research Communications 354 585–590. Zhou T. 2007. A complex system of small RNAs in the unicellular green alga Chlamydomonas reinhardtii. Genes Development 21 1190–1203. Zhou M. Li D. Li Z. Hu Q. Yang C. Zhu L. et al. 2013. Constitutive expression of a miR319 gene alters plant develop- ment and enhances salt and drought tolerance in transgenic creeping bentgrass. Plant Physiology 161 1375–1391. 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 10 61–75. Zhou C. Zhang L. Duan J. Miki B. Wu K. 2005. HISTONE DEACETYLASE19 is involved in jasmonic acid and ethylene signaling ofpathogenresponsein Arabidopsis. Plant Cell174 1196–1204. Zhu J. Kapoor A. Sridhar V. V. Agius F. Zhu J. K. 2007a. The DNA glycosylase/lyase ROS1 functions in pruning DNA methylation patternsin Arabidopsis. Current Biology 1754–59. Zhu J. K. Zhu J. Hu X. Zhu J. 2007b. Role of microRNA in plant salt tolerance. United States Patent 20070214521. Ind J Plant Physiol. October–December 2017 224:458–469 469 123 Authors personal copy

authorStream Live Help