Park, J. E. et al. GH3-mediated auxin homeostasis links growth regulation with stress adaptation response in Arabidopsis. J. Biol. Chem. 282, 10036-10046

Department of Agronomy and Horticulture, University of Nebraska at Lincoln, Lincoln, Nebraska, United States
Journal of Biological Chemistry (Impact Factor: 4.57). 04/2007; 282(13):10036-46. DOI: 10.1074/jbc.M610524200
Source: PubMed


Plants constantly monitor environmental fluctuations to optimize their growth and metabolism. One example is adaptive growth occurring in response to biotic and abiotic stresses. Here, we demonstrate that GH3-mediated auxin homeostasis is an essential constituent of the complex network of auxin actions that regulates stress adaptation responses in Arabidopsis. Endogenous auxin pool is regulated, at least in part, through negative feedback by a group of auxin-inducible GH3 genes encoding auxin-conjugating enzymes. An Arabidopsis mutant, wes1-D, in which a GH3 gene WES1 is activated by nearby insertion of the (35)S enhancer, exhibited auxin-deficient traits, including reduced growth and altered leaf shape. Interestingly, WES1 is also induced by various stress conditions as well as by salicylic acid and abscisic acid. Accordingly, wes1-D was resistant to both biotic and abiotic stresses, and stress-responsive genes, such as pathogenesis-related genes and CBF genes, were upregulated in this mutant. In contrast, a T-DNA insertional mutant showed reduced stress resistance. We therefore propose that GH3-mediated growth suppression directs reallocation of metabolic resources to resistance establishment and represents the fitness costs of induced resistance.

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    • "To test this hypothesis two distinct environmental growth perturbations were chosen to investigate their effect on IAA homeostasis mediated by the GH3 family in P. patens based on previous reports that IAA and its conjugates could be connected. (a) Elevated temperatures because it was shown that they were related to increased auxin in two different plant species (Oetiker and Aeschbacher, 1997; Gray et al., 1998), and because gh3.5 mutants of Arabidopsis were more susceptible to elevated temperatures (Park et al., 2007a). (b) Darkness, because another Arabidopsis GH3 gene was involved in light-dependent growth. "
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    ABSTRACT: Two proteins of the GRETCHEN HAGEN3 (GH3) family of acyl acid amido synthetases from the moss Physcomitrella patens conjugate indole-3-acetic acid (IAA) to a series of amino acids. The possible function of altered auxin levels in the moss in response to two different growth perturbations, elevated temperatures and darkness, was analyzed using a) the recently described double knockout lines in both P. patens GH3 genes (GH3-doKO) and b) a previously characterized line harboring an auxin-inducible soybean GH3 promoter::reporter fused to β-glucuronidase (G1-GUS). The GUS activity as marker of the auxin response increased at higher temperatures and after cultivation in the darkness for a period of up to four weeks. Generally, the double knockout plants grew more slowly than the wild type (WT). The altered growth conditions influenced the phenotypes of the double knockout lines differently from that of WT moss. Higher temperatures negatively affected GH3-doKO plants compared to WT which was shown by stronger loss of chlorophyll. On the other hand, a positive effect was found on the concentrations of free IAA which increased at 28 °C in the GH3-doKO lines compared to WT plants. A different factor, namely darkness vs. a light/dark cycle caused the adverse phenotype concerning chlorophyll concentrations. Mutant moss plants showed higher chlorophyll concentrations than WT and these correlated with higher free IAA in the plant population that was classified as green. Our data show that growth perturbations result in higher free IAA levels in the GH3-doKO mutants, but in one case - growth in darkness - the mutants could cope better with the condition, whereas at elevated temperatures the mutants were more sensitive than WT. Thus, GH3 function in P. patens WT could lie in the regulation of IAA concentrations under unfavorable environmental conditions.
    Plant Physiology and Biochemistry 11/2015; 97:339-349. DOI:10.1016/j.plaphy.2015.10.013 · 2.76 Impact Factor
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    • "Morphological adaptations, such as the development of a waxy cuticle, vasculature, stomata, more complex root systems, and a diverse set of molecular mechanisms, allow plants to live in sometimes extreme conditions. Numerous studies have elucidated the adaptations of plants to severe drought conditions (McDowell et al., 2008; Akhtar et al., 2012; Golldack et al., 2014), often by withholding water until wilting or by cutting leaves and letting them dry to impose severe water deficits (Iuchi et al., 2001; Llorente et al., 2002; Taji et al., 2002; Cheong et al., 2003, 2007; Tran et al., 2004; Umezawa et al., 2004, 2006; Cominelli et al., 2005; Chen et al., 2006; Nelson et al., 2007; Park et al., 2007; Zhu et al., 2007; Zhang et al., 2008). However, the sudden infliction of such severe drought is unlikely to reflect what naturally happens in the field. "
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    ABSTRACT: Although the response of plants exposed to severe drought stress has been studied extensively, little is known about how plants adapt their growth under mild drought stress conditions. Here, we analyzed the leaf and rosette growth response of six Arabidopsis thaliana accessions originating from different geographic regions, when exposed to mild drought stress. The automated phenotyping platform WIWAM was used to impose stress early during leaf development, when the third leaf emerges from the shoot apical meristem. Analysis of growth related phenotypes showed differences in leaf development between the accessions. In all six accessions, mild drought stress reduced both leaf pavement cell area and number, without affecting the stomatal index. Genome-wide transcriptome analysis (using RNA sequencing) of early developing leaf tissue identified 354 genes differentially expressed under mild drought stress in the six accessions. Our results indicate the existence of a robust response over different genetic backgrounds to mild drought stress in developing leaves. The processes involved in the overall mild drought stress response comprised abscisic acid signaling, proline metabolism and cell wall adjustments. In addition to these known severe drought related responses, 87 genes were found to be specific for the response of young developing leaves to mild drought stress. Copyright © 2015, American Society of Plant Biologists.
    Plant physiology 01/2015; 167(3). DOI:10.1104/pp.114.254284 · 6.84 Impact Factor
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    • "Moreover, while overexpression ofAtGH3.5 increases level of IAA accumulation (Zhang et al. 2007), the gain-of-function mutant of AtGH3.5 also elevates SA accumulation and increases expression of PATHOGENESIS-RELATED PROTEIN 1 (PR-1) in response to biotic stress. While experiments with above mutants demonstrate that amino acid conjugates of SA by auxin upregulated GH3 proteins can act as a bioactive trigger of plant pathogen defense responses (Park et al. 2007). "
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    ABSTRACT: Plant hormones operate in a very complex network where they regulate and control different vital mechanisms. They coordinate growth, development and defense via signaling involving different interactions of molecules. Activation of molecules responsible for regulation of plant immunity is mainly provided by salicylic and jasmonic acid signaling pathways. Similar to the signaling of these defense-associated plant hormones, auxin can also affect resistance to different pathogen groups and disease is manifested indirectly through the effects on growth. The various ways in which auxin regulate growth and plant development and might be closely connected to plant defense, are discussed in this review.
    Biologia 10/2014; 69(10). DOI:10.2478/s11756-014-0431-3 · 0.83 Impact Factor
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