From Laboratory to Field. Using Information from Arabidopsis to Engineer Salt, Cold, and Drought Tolerance in Crops

Abstract

After almost a century since its first appearance in the scientific literature, Arabidopsis has now been widely adopted as a model plant of choice for biological research (Somerville and Koornneef, 2002). Its many advantages include a small genome, short life cycle, small stature, prolific seed production, and ease of transformation. In addition, a wealth of genomics resources exists, such as a completely sequenced genome, a near saturation insertion mutant collection, a genome array that contains the entire transcriptome, and more than 50,000 molecular markers. Add in a vibrant collaborative community, and it is easy to see why Arabidopsis is often the system of choice for plant research. While the culminating achievement of Arabidopsis research—the release of its complete genome sequence—is still fresh in memory, a new 10-year project of comparable importance has already begun. The ambitious goal of this program is to know the function of all Arabidopsis genes by 2010 (Somerville and Dangl, 2000). This knowledge will facilitate the development of a virtual plant—a computer model that will use information about each gene product to simulate the growth and development of a plant under many environmental conditions. However, it has not escaped many plant biologists that another goal is to use knowledge gained from research on Arabidopsis to facilitate the understanding of biological phenomena in other plant species. One specific challenge is how to utilize information gained from Arabidopsis research to produce new commercial plant varieties. In this perspective, we reflect on the critical role Arabidopsis is playing in unraveling abiotic stress signal transduction (focusing primarily on salt, cold, and drought stress), and how these new insights on the mechanisms of tolerance to these stresses are suggesting novel approaches to engineer the next generation of biotech crops. The SOS signaling pathway for the regulation of Na+ homeostasis and salt tolerance in Arabidopsis. High Na+ stress triggers a calcium signal that activates the SOS3-SOS2 protein kinase complex, which then stimulates the Na+/H+ exchange activity of SOS1 at the plasma membrane. SOS2 also activates Na+/H+ (AtNHX) and Ca2+/H+ (CAX1) exchangers on the vacuolar membrane. The protein phosphatase ABI2 has been shown to physically interact with SOS2 and is proposed to inactivate SOS2. The SOS pathway may down-regulate the activity of Na+ influx transporters (AtHKT1 and NCS). SOS1 in gray indicates that this transporter may also have a sensory role. Dotted lines indicate possible regulation. Readers are referred to a recent publication for an extensive review of the regulation of ion homeostasis under salt stress (Zhu, 2003). It is noteworthy that Arabidopsis has played a vital role in many investigations of the basic processes that occur during salt stress. For example, SOS1/2/3 were identified by Arabidopsis mutants and position-based cloning (Liu and Zhu, 1998; Liu et al., 2000; Shi et al., 2000); AtNHX1 was discovered from Arabidopsis genome sequences (Apse et al., 1999; Gaxiola et al., 1999); and HKT1, initially identified in wheat (Triticum aestivum; Schachtman and Schroeder, 1994), has been shown through the study of Arabidopsis knockout mutants to be an important Na+ influx system in plant roots (Rus et al., 2001) and to play a critical role in controlling the long distance transport of Na+ (Maser et al., 2002; Berthomieu et al., 2003). These and other examples illustrated how mutant isolation, position-based cloning, and gene expression analysis in Arabidopsis can be combined with biochemical and physiological studies to unravel the inner workings of salt stress signal transduction (Zhu, 2002). It is generally accepted that maintaining a low cytosolic Na+ concentration is essential to achieve salt tolerance and can be achieved by restricting inflow, increasing outflow, or increasing vacuole sequestration of Na+. Intuitively, increasing plasma membrane Na+ exporters and tonoplast Na+ importers and/or restricting the amount of Na+ influx by lowering the amount of plasma membrane Na+ importers should suffice. Indeed, a number of successes have ensued when these strategies were used (see Table I Engineered abiotic stress tolerance: from ion transporters to transcription factors Engineered abiotic stress tolerance: from ion transporters to transcription factors Transcriptional cascades of low temperature and dehydration signal transduction. ABA-dependent transcriptional factors are shaded, while ABA independent factors are not. Small circles indicate posttranscriptional modification, such as phosphorylation. Transcription factor binding sites are represented as rectangles at the bottom of the figure, with the representative promoters listed below. Dotted lines indicate possible regulation. Double arrow lines indicate possible cross talk. The regulation of gene expression by ABA has been reviewed in great detail elsewhere (Finkelstein et al., 2