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Rice requires an optimal range of temperature for growth and development. But higher temperature than the threshold will be available option for rice growth in future. The high temperature (HT) put considerable impact on the productivity and yield. So, in order to make rice crop better tolerant to HT, crucial components that confers tolerance to HT stress need to be explored. The microRNAs (miRNA) are one such category evidenced to be one of the crucial components in plant system under HT stress that responds via up-or down-regulation of themselves and regulation of the respective target genes. These finding suggests that investigating these HT stress-responsive miRNAs may reveals the regulatory mechanisms that control rice growth and development under HT stress condition. Here, evidence related to the connection between the miRNAs in imparting HT tolerance in rice has been investigated that may help in providing clues for developing HT-tolerant rice.

Rice is one of the major food crops across the world and an increase in its production is necessary to satisfy the future needs. The rice plant requires different critical temperature at different growth stages such as germination, vegetative, or reproductive stage (Yoshida, 1981). Deviation from the optimal or threshold temperature quenches the rice’s normal growth and development and thus productivity of rice crops (Yoshida, 1981; Welch et al., 2010). However, effects of heat or High Temperature (HT) are reported to be different on different rice genotypes. For instance, effect of HT at the anthesis (most temperature sensitive stage of rice), in three rice (Oryza sativa L.) genotypes showed that out of three, N22 (71%) was the highly tolerant genotype of rice (Jagadish et al., 2010). Further, transgenic rice, NH219 mutant was showed to be more tolerant than wild type N22 to heat stress because its percent yield reduction was lesser than N22 (Poli et al., 2013).

Now, what crucial components involved High-Temperature-Tolerant (HTT) rice genotype confers tolerance to HT is an active area for research. Evidence shows miRNAs to be potential candidate that have crucial role imparting in HT response by plants. In this review the evidence related to the connection between the miRNAs in imparting HT tolerance in rice has been investigated.
HT-Responsive miRNAs

Although, the HT-Responsive (HTR) miRNAs reported in some plants such as Populus, Wheat, Brassica rapa, and Rice (Jeong et al., 2011; Xin et al., 2010; Yu et al., 2011, Sailaja et al, 2014), but extensive studies across plant species are still needed. So, in the following sections different HTR miRNAs, targets, genes and responses are summarized to foster the further investigation in this area.

HTR miRNAs: miR398, miR156, miR162 and miR167 show similar expression pattern.

HTR miRNA, miR398, miR156, miR162 and miR167 showed to be down-regulation in both roots and shoots rice seedling (Sailaja et al, 2014). This suggests that they have important roles in regulation under HT stress. The miRNAs-target relationship shows a negative correlation between them most of the time except few. For instance, under HT while miR156 targets were up-regulated, their targets SPL2 were down-regulated (Xin et al., 2010; Yu et al., 2011). Also, recent finding identified that HTR miR398 target Cu/Zn superoxide dismutase were up-regulated while itself was down-regulated (Yu et al., 2011; Sailaja et al, 2014).

HTR miRNA: miR169, miR1884 and miR160 showed differential expression pattern. Real time PCR miRNA expression studies have showed that most of the miRNAs were down-regulated under HT. In addition to this, some of them were differentially expressed in roots and shoots at HT. For instance, miR169, miR1884 and miR160 were up-regulated in shoots and down regulated in roots (Sailaja et al, 2014). Further, miR1884 responds differently to cold stress i.e. in rice shoots, they were down-regulated under cold stress (Lu et al, 2010). So, miR1884 represents a key regulator in rice temperature stress response because of its differential expression under cold and HT in different rice plant tissues. Another, HTR miRNA, miR160 impart regulatory role via auxin signaling pathway through transcription factors (Rhoades et al, 2002). Xin et al (2010) previously also reports the similar HTR miR160 up-regulation in wheat.

Connection between HTR miRNAs (miR-168a and miR-408) and Ca2+/ calmodulin (CaM) exist. Ca2+ level are change in response to HT stresses which in turn affects the calmodulin (CaM). For example, a recent study indicates that the predicted target of miR388 to be CAM (Sailaja et al, 2014).

In addition to this, experimental study showed that CaM1-1 posses differential miRNAs (miR-168a and miR-408) target sites and these miRNAs posses heat responsive cis-elements suggesting that these miRNAs are involved in CaM1 regulation during HT stress at post-transcriptional level (Wu and Jinn, 2012). Therefore, miRNAs represents crucial component in regulating these Ca2+/calmodulin (CaM) signalling pathway that in turn play important role during HT stress and in further acquiring thermo-tolerance in plants.

Connection between HTR miRNA (miR-398) and Cu/Zn superoxide dismutase-coding (CSD) gene exist.

Rapid accumulation of ROS such as hydrogen peroxide (H2O2) has been in response to HT stress which in turn causes oxidative stress (Halliwell, 2006; Hasanuzzaman et al., 2013; Liu and Huang, 2000). Superoxide dismutase (SOD) is an important ROS scavenging enzyme and thus provide defense against oxidative stress to some extent (Fridovich, 1995) and

Cu/Zn-SOD, also known as CSD is one type of SOD.

miR398 has highly conserved binding sites in mRNAs chaperone and SOD orthologs in plants that were diverged more than million years ago (Bari, Berillo, Orazova, and Ivashchenko, 2013). In addition to this, HTR miR398 targets Cu/Zn superoxide dismutase were up-regulated while itself was down-regulated (Yu et al., 2011; Sailaja et al, 2014; Sunkar et al., 2006).

Transgenic plants over expressing  miR398-resistant form of CSD2 were showed to be more sensitive to heat stress than transgenic plants over expressing normal coding sequence of CSD2 (Lu, Guan and Zhu, 2013; Sunkar et al., 2006). Thus the down regulation of CSD2 mediated by the heat-inducible miR398 imparts required thermo-tolerance in Arabidopsis. In addition to this,

Connection between heat shock proteins (HSPs) and HTR miRNAs (miR168) exist.

Heat shock proteins (HSPs) are crucial in imparting tolerance to plants as their expression are induced under HT that regulate or suppress the synthesis of normal cellular proteins (Chang et al., 2012). For instance HSP101 was shown to important role in heat tolerance in Arabidopsis (Queitsch et al, 2000). Further, HSPs rapid accumulation in the HT sensitive plant organs can imparts protection of the cell’s metabolic apparatus. Therefore, they are crucial components in better adaptation and survival of under HT (Wahid et al., 2007). Therefore, increased HTR HSPs accumulation play a crucial role in protecting metabolic activities of the cell and is a key component for plants adapting to heat (Jagadish et al., 2010). For instance, at HT, cold (CSP) and heat shock proteins (HSP) were significantly up-regulated and the Fe-deficiency proteins were shown to be down-regulated in the heat-tolerant genotype, N22, as compared to wild type (Jagadish et al., 2010). So, both CSP and HSP HTRs in the anthers are suggested to be function in imparting greater tolerance to N22 genotype. Along with this, heat stress transcription factors (HSFs) and heat shock proteins (HSPs) expressions were reduced in the heat-sensitive miR398-resistant form of CSD2 transgenic plants (Lu, Guan and Zhu, 2013).

Besides these, computational predictions also indicate the involvement of miRNAs in regulating HSPs. For example, it has been predicted that the target of miR414 were predicted as HSP70 and HSP 81-1 and miR399b, 399e targets HSP binding proteins (Sailaja et al, 2014). Therefore, these HSPs expression related to miRNAs in response to HT stress could help in understanding the mechanism that can provide tolerance to rice plant under HT.

Relationship of HTR rice miRNAs in High-Temperature-Tolerance

High-Temperature-Tolerant (HTT) rice can be defined as the rice plant ability to grow and produce efficiently under HT stress (Wahid et al., 2007). Developing HTT rice depends on factors such as the panicle emergence time and spikelet/floret opening relative to the time of stress occurrence and tolerance of anther dehiscence to the stress.

Plants inherent ability to tolerate HT for growth is termed as Basal thermo-tolerance (BTT) (Larkindale et al., 2005; Lee et al., 1995). They also have ability to acquire tolerance to lethal HT called as acquired or induced thermo-tolerance (ATT) (Larkindale et al., 2005; Burke et al., 2000). ATT depend on two factors one induction of specific pathways during the acclimation period, second subsequent acquisition of thermo-tolerance. The study of HTT in rice during flowering is difficult because Quantitative trait loci (QTL) studies have shown that it is under polygenic control (Zhang et al., 2009).

Researches on how miRNAs in rice help it to respond to HT stress can improve our understanding about its transcriptional, post-transcriptional and other related mechanisms under the HT stress. Both experimental identification as well as computational efforts is proceeding. With the discoveries of HTR miRNAs mediated regulation of crucial HTR genes like CIPK, CaM, ROS, CSD and HSPs helps in fostering our understanding about complex mechanism involve in heat response and heat tolerance to rice plants. In addition to this, several pathways are showed to be involved in HT response like auxin signaling pathways and calcium signaling pathways while other involved through cascade of responses. Further, HTR miRNA and their target genes are potential candidates that can be used for transgenic research for developing HT-tolerant rice plant.Therefore, further uncovering complex HTR mechanism in rice and the role of key components like HTR miRNAs and their target genes in rice that are involved in signal transduction pathways may reveal the approach through which HTT rice can be developed in future with miRNAs playing central role.


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Divyesh D.Sanghani

Lecturer in Department of Commerce –Saurashtra University



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