A nucleotide metabolite controls stress-responsive gene expression and plant development.
A nucleotide metabolite controls stress-responsive gene expression and plant development.
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DOI：
10.1371/journal.pone.0026661
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发表时间：
2011
期刊：
影响因子：
3.7
通讯作者：
Xiong L
中科院分区：
文献类型：
--
作者：
Chen H;Zhang B;Hicks LM;Xiong L
非生物胁迫，如干旱和高盐，激活了一个信号级联网络，导致许多胁迫响应基因在植物中的表达。拟南芥FIERY 1（FRY 1）蛋白是逆境和脱落酸（阿坝）信号的负调节因子，在体外具有肌醇多磷酸酶和3′，5 ′-二磷酸核苷酸酶活性。FRY 1核苷酸酶降解硫酸化副产物3′-磷酸腺苷-5 ′-磷酸（PAP），但其体内功能，特别是其在应激基因调控中的作用仍不清楚。在这里，我们开发了一种LC-MS/MS方法来定量测量植物中PAP水平，并研究了这种核苷酸酶活性在胁迫反应和植物发育中的作用。结果发现，PAP水平在植物中受到严格控制，并且在正常条件下或在NaCl、LiCl、冷或阿坝处理下均未积累到任何显著水平。与此相反，高水平的PAP检测在多个突变等位基因的FRY 1，但不是在其他FRY 1家族成员的突变体，表明FRY 1是主要的酶，水解PAP在体内。我们通过过表达酵母PAP核苷酸酶或产生PAP前体3′-磷酸腺苷-5 ′-磷酸硫酸盐（PAPS）生物合成缺陷的fry 1 apk 1 apk 2三重突变体，在遗传上降低了fry 1突变体中的PAP水平，证明了fry 1突变体中的发育缺陷和胁迫响应基因的超诱导与植物中PAP的积累相关。我们还发现，在fry 1中的过敏性应激基因的调控需要ABH 1，而不是ABI 1，阿坝信号通路中的另外两个负调控因子。然而，与酵母不同，拟南芥中FRY 1的过表达不能增强耐盐性。两者合计，我们的研究结果表明，PAP是关键的胁迫基因调控和植物发育，但FRY 1核苷酸酶分解代谢PAP可能不是在拟南芥体内盐毒性的目标。
Abiotic stress, such as drought and high salinity, activates a network of signaling cascades that lead to the expression of many stress-responsive genes in plants. The Arabidopsis FIERY1 (FRY1) protein is a negative regulator of stress and abscisic acid (ABA) signaling and exhibits both an inositol polyphosphatase and a 3′,5′-bisphosphate nucleotidase activity in vitro. The FRY1 nucleotidase degrades the sulfation byproduct 3′-phosphoadenosine-5′-phosphate (PAP), yet its in vivo functions and particularly its roles in stress gene regulation remain unclear. Here we developed a LC-MS/MS method to quantitatively measure PAP levels in plants and investigated the roles of this nucleotidase activity in stress response and plant development. It was found that PAP level was tightly controlled in plants and did not accumulate to any significant level either under normal conditions or under NaCl, LiCl, cold, or ABA treatments. In contrast, high levels of PAP were detected in multiple mutant alleles of FRY1 but not in mutants of other FRY1 family members, indicating that FRY1 is the major enzyme that hydrolyzes PAP in vivo. By genetically reducing PAP levels in fry1 mutants either through overexpression of a yeast PAP nucleotidase or by generating a triple mutant of fry1 apk1 apk2 that is defective in the biosynthesis of the PAP precursor 3′-phosphoadenosine-5′-phosphosulfate (PAPS), we demonstrated that the developmental defects and superinduction of stress-responsive genes in fry1 mutants correlate with PAP accumulation in planta. We also found that the hypersensitive stress gene regulation in fry1 requires ABH1 but not ABI1, two other negative regulators in ABA signaling pathways. Unlike in yeast, however, FRY1 overexpression in Arabidopsis could not enhance salt tolerance. Taken together, our results demonstrate that PAP is critical for stress gene regulation and plant development, yet the FRY1 nucleotidase that catabolizes PAP may not be an in vivo salt toxicity target in Arabidopsis.
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