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Plant Physiology 140:1139-1141 (2006) © 2006 American Society of Plant Biologists Abiotic Stress in Rice. An "Omic" ApproachUniversity of Illinois, Urbana, IL
Abiotic stress can impose limitations on crop productivity and also limit land available for farming, often in regions that can ill afford such constraints, thus highlighting a greater need for understanding how plants respond to adverse conditions with the hope of improving tolerance of plants to environmental stress. More is becoming known about the physiological and molecular effects of environmental stress, and many groups are turning to "omic" studies with the goal of identifying the genes involved and their expression patterns during the course of stress perception and response. If analyzed properly, the information gleaned from these studies will help identify the interactions between signaling pathways, along with novel cis-acting elements, in the promoters of coregulated genes (Provart and McCourt, 2004
As sessile organisms, plants cannot physically move away from environmental stresses that can negatively affect growth. Therefore, plants have had to evolve strategies to cope with abiotic stress. Indeed, the ability to respond and ultimately adapt to abiotic stress may be a driving force in speciation (for review, see Lexer and Fay, 2005  ). Plants must be able to "sense" the environmental cues before being able to respond appropriately to the abiotic stress. Due to the complex nature of stress, multiple sensors, rather than a single sensor, are more likely to be responsible for perception of the stress. After the initial recognition of the stress, a signal transduction cascade is invoked. Secondary messengers relay the signal, ultimately activating stress-responsive genes generating the initial stress response. Stress-induced gene products can be divided into two major groups: those involved in stress tolerance and those involved in signal transduction. Stress-tolerance genes enable plants to cope with the stress situation, in terms of both short- and long-term responses. These can include the synthesis of chaperones and enzymes for osmolyte biosynthesis and detoxification, to a change in the composition of membrane lipids as is found with cold stress. Gene products can also act as transcription regulators controlling sets of stress-specific genes or be involved in the production of regulatory molecules, such as the plant hormone ABA.
It has been demonstrated that multiple signaling pathways can be activated during exposure to stress, leading to similar responses to different triggers. For example, drought, low temperature, and high salinity, three common abiotic stresses, all cause an accumulation of compatible solutes and antioxidants (Hasegawa et al., 2000
In their study, Rabbani et al. (2003) used microarray analysis to determine rice genes induced by the stresses of cold, drought, high salinity, and by the hormone ABA, a regulatory molecule generated by stress. The accuracy of the transcriptome data was confirmed by RNA gel-blot analysis of candidate genes, narrowing it to 73 genes up-regulated by exposure to the abiotic stress. Of these, 20% are already known to be responders to abiotic stress in rice, confirming their up-regulation during stress exposure. Among these were those involved in stress tolerance, such as compatible solutes and proteins involved in carbohydrate metabolism and detoxification, and those involved in regulation, such as transcriptions factors. Additionally, a gene involved in the biosynthesis of ABA was also identified. This is interesting, as ABA is known to be a regulatory molecule in stress response and functions to regulate plant water balance through guard cells as well as regulate osmotic stress tolerance via cellular dehydration tolerance genes. The remaining 80% have not previously been reported as stress responders in rice. One objective of this experiment was to identify cis-acting elements involved in stress-inducible gene expression. These regulatory elements interact with transcription factors and act as molecular "switches" ensuring an appropriate response (in this instance, to environmental stress). In Arabidopsis (Arabidopsis thaliana), for example, the dehydration-responsive element has been identified as a cis-acting promoter element and has been implicated in regulating gene expression under drought, high-salinity, and cold stress. To determine how many of the candidate rice genes contained a dehydration-responsive element or an ABA-responsive element, the 5'-end sequences were compared to rice genomic sequences in both the GenBank and Rice Genome Project databases in order to obtain the complete coding sequence. The complete genomic sequences of 95% of the identified stress-responsive genes were present in the databases, allowing analysis of the promoter regions. Of these, almost 40% contained a dehydration-responsive element or ABA-responsive elements in their promoter region. The authors interpreted the lack of either element in the remaining 60% to suggest the presence of novel cis-acting elements. Cross talk between the abiotic-stress responses was also explored, revealing a high degree of similarity. Specifically, drought and salt stress were found to induce many of the same genes as did drought stress and ABA application. The similarity between drought and high-salinity response in rice also has been observed in Arabidopsis. Plant response to drought and salt stress is very similar, with both disrupting the ion and osmotic homeostasis of the plant, thus the signaling pathways would be expected to be similar. Both drought and salt stress result in increase in ABA expression, known to be involved in the tolerance of osmotic stress and regulation of plant water balance, where it is involved in guard cell regulation. This is illustrated in ABA-deficient mutants that grow relatively normally unless they are exposed to water stress. Under drought conditions, these plants rapidly wilt and will die if the stress remains. Contrary to what was seen with drought and high salinity, the overlap between the cold and high-salinity stress responses or cold and ABA application was not that high.
NAC domain-containing proteins are members of a large family of plant-specific transcription factors, of which only a small fraction has assigned function. These functions are diverse and are believed to be involved in defense, development, and abiotic-stress response (for review, see Olsen et al., 2005 ). Nogueira et al. (2005) identified 26 nonredundant NAC genes from sugarcane (Saccharum officinarum), including SsNAC23, which was previously shown to be up-regulated by cold (Nogueira et al., 2003). Molecular modeling of SsNAC23 predicts it to contain a basic amino acid-rich protrusion, a conserved characteristic of NAC domain transcription factors, while transient  -glucuronidase fusion studies suggest targeting to the nucleus. Taken together, this supports the idea of SsNAC23 being a transcription factor. SsNAC23 is orthologous to rice OsNAC6 (Kikuchi et al., 2000) and is strongly induced by extreme chilling stress and transiently by water stress and herbivory. In rice, NAC6 expression was found to increase slowly after cold exposure (Rabbani et al., 2003). The induction of SsNAC by these stresses is in line with the known function of NAC domain-containing proteins. Osmocant-induced water stress also induced expression similar to what was observed with OsNAC6 (Rabbani et al., 2003), but, unlike what was observed in rice, it did not respond to exogenous application of ABA.
Basic region/Leu zipper (bZIP) proteins are a family of transcription factors that, as their name implies, contain a region of basic amino acids followed by a region containing at least three to four repeats of Leu or another hydrophobic amino acid. The hydrophobic region mediates homodimer formation, whereas the basic area is involved in DNA binding, usually to an ACGT sequence. A notable exception is the oncogene Fos, which does not bind to DNA but rather binds to another bZIP protein (Jun) to produce heterodimers. The cold-induced plant bZIP protein LIP19 (Aguan et al., 1993
The transcriptome profiling of rice seedlings by Rabbani et al. (2003 ) has added to the foundation necessary for further understanding of how plants respond to abiotic stress. As brought up in this article, transcriptome profiling provides the ability to identify novel cis-acting elements and elements acting in tandem. As this field is further advanced, the accuracy of transcript profiling will become increasingly exact, allowing the pattern of the complex web of signaling to be uncovered.
www.plantphysiol.org/cgi/doi/10.1104/pp.104.900188.
Aguan K, Sugawara K, Suzuki N, Kusano T (1993) Low-temperature-dependent expression of a rice gene encoding a protein with a leucine-zipper motif. Mol Gen Genet 240: 1–8[CrossRef][Web of Science][Medline] Hasegawa PM, Bressan RA, Zhu JK, Bohnert HJ (2000) Plant cellular and molecular responses to high salinity. Annu Rev Plant Physiol Plant Mol Biol 51: 463–499[CrossRef][Web of Science] Kikuchi K, Ueguchi-Tanaka M, Yoshida KT, Nagato Y, Matsusoka M, Hirano H-Y (2000) Molecular analysis of the NAC gene family in rice. Mol Gen Genet 262: 1047–1051[CrossRef][Web of Science][Medline] Lexer C, Fay MF (2005) Adaptation to environmental stress: a rare or frequent driver of speciation? J Evol Biol 18: 893–900[Medline] Nogueira FTS, De Rosa VE, Menossi M, Ulian EC, Arruda P (2003) RNA expression profiles and data mining of sugarcane response to low temperature. Plant Physiol 132: 1811–1824 Nogueira FTS, Schlogl PS, Camargo SR, Fernandez JH, De Rosa VE, Pompermayer P, Arruda P (2005) SsNAC23, a member of the NAC domain protein family, is associated with cold, herbivory and water stress in sugarcane. Plant Sci 169: 93–106[CrossRef] Olsen AN, Ernst HA, Lo Leggio L, Skiver K (2005) NAC transcription factors: structurally distinct, functionally diverse. Trends Plant Sci 10: 79–87[CrossRef][Web of Science][Medline] Provart NJ, McCourt P (2004) Systems approaches to understanding cell signaling and gene regulation. Curr Opin Plant Biol 7: 605–609[Medline] Rabbani MA, Maruyama K, Abe H, Khan MA, Katsura K, Ito Y, Yoshiwara K, Seki M, Shinozaki K, Yamaguchi-Shinozaki K (2003) Monitoring expression profiles of rice genes under cold, drought, and high-salinity stresses and abscisic acid application using cDNA microarray and RNA get-blot analyses. Plant Physiol 133: 1755–1767 Shimizu H, Sato K, Berberich T, Miyazaki A, Ozaki R, Imai R, Kusano T (2005) LIP19, a basic region leucine zipper protein, is a Fos-like molecular switch in the cold signaling of rice plants. Plant Cell Physiol 46: 1623–1634
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