Threshold-dependent repression of SPL gene expression by miR156/miR157 controls vegetative phase change in Arabidopsis thaliana.
Threshold-dependent repression of SPL gene expression by miR156/miR157 controls vegetative phase change in Arabidopsis thaliana.
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DOI：
10.1371/journal.pgen.1007337
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发表时间：
2018-04
期刊：
影响因子：
4.5
通讯作者：
Poethig RS
中科院分区：
文献类型：
--
作者：
He J;Xu M;Willmann MR;McCormick K;Hu T;Yang L;Starker CG;Voytas DF;Meyers BC;Poethig RS
营养阶段的变化是由miRNAs、miR156和miR157丰度的降低以及由此导致的其靶标--鳞状启动子结合蛋白样转录因子(SPL)表达的增加来调节的。为了确定miR156/miR157如何确定营养阶段发生的叶片形态的数量和质量变化，我们测量了它们在连续叶片中的丰度，并表征了不同miR156和MIR157基因突变的表型。MiR156/miR157在第1、2叶和第3叶之间下降较快，此后下降较慢。叶片1和2中miR156/miR157的含量大大超过了确定其身份所需的阈值。后续叶片的miR156/miR157水平相对较低，对其丰度的微小变化很敏感。在这些后期形成的叶片中，miR156/miR157的数量接近确定幼虫与成虫身份所需的阈值；这些叶片中miR156/157丰度的相对较小的下降会导致SPL蛋白的不成比例的大幅增加和叶片形态的显著变化。MiR157比miR156更丰富，但对新梢形态和Spl基因表达的影响比miR156小。这可能是由于miR157被装载到Ago1上的效率低下，以及在miR157：SPL13双链中miR157的5‘端存在额外的错配核苷酸。MiR156通过不同的机制抑制不同的靶点：它通过转录切割和翻译抑制相结合的方式调节SPL9，主要通过翻译抑制来调节SPL13。我们的结果为拟南芥新梢发育过程中叶片形态的变化提供了分子解释，并为miR156和miR157调控基因表达的机制提供了新的见解。在拟南芥新梢发育的不同阶段产生的叶片在形状和大小上是可以预测的。以前的研究表明，这一现象受miRNAs、miR156和miR157丰度的变化调节，但miR156/miR157如何引起新梢发育过程中叶片形态的变化尚不清楚。为了回答这个问题，我们测量了miR156/miR157及其SPL靶标在连续的叶原基中的丰度，并表征了miR156/miR157丰度的变化对叶片形态以及SPL转录本和SPL蛋白丰度的影响。MiR156/miR157在头两片莲座状叶片中含量很高，在那里它们作为缓冲来稳定叶片的特性。它们在随后的叶片中以较低的水平存在并稳步下降，在那里它们起到调节叶片形态发生的作用。在这些后期形成的叶片中，miR156/miR157丰度的微小下降会导致SPL活性的不成比例的大幅增加，这主要是由于SPL转录本的翻译增加所致。我们的结果为研究拟南芥营养阶段的变化以及miR156和miR157调控这一过程的机制提供了新的视角。
Vegetative phase change is regulated by a decrease in the abundance of the miRNAs, miR156 and miR157, and the resulting increase in the expression of their targets, SQUAMOSA PROMOTER BINDING PROTEIN-LIKE (SPL) transcription factors. To determine how miR156/miR157 specify the quantitative and qualitative changes in leaf morphology that occur during vegetative phase change, we measured their abundance in successive leaves and characterized the phenotype of mutations in different MIR156 and MIR157 genes. miR156/miR157 decline rapidly between leaf 1&2 and leaf 3 and decrease more slowly after this point. The amount of miR156/miR157 in leaves 1&2 greatly exceeds the threshold required to specify their identity. Subsequent leaves have relatively low levels of miR156/miR157 and are sensitive to small changes in their abundance. In these later-formed leaves, the amount of miR156/miR157 is close to the threshold required to specify juvenile vs. adult identity; a relatively small decrease in the abundance of miR156/157 in these leaves produces a disproportionately large increase in SPL proteins and a significant change in leaf morphology. miR157 is more abundant than miR156 but has a smaller effect on shoot morphology and SPL gene expression than miR156. This may be attributable to the inefficiency with which miR157 is loaded onto AGO1, as well as to the presence of an extra nucleotide at the 5' end of miR157 that is mis-paired in the miR157:SPL13 duplex. miR156 represses different targets by different mechanisms: it regulates SPL9 by a combination of transcript cleavage and translational repression and regulates SPL13 primarily by translational repression. Our results offer a molecular explanation for the changes in leaf morphology that occur during shoot development in Arabidopsis and provide new insights into the mechanism by which miR156 and miR157 regulate gene expression. Leaves produced at different stages in the development of an Arabidopsis shoot vary predictably in shape and size. Previous studies have shown that this phenomenon is regulated by variation in the abundance of the miRNAs, miR156 and miR157, but how miR156/miR157 produce the changes in leaf morphology that occur during shoot development is not understood. To answer this question, we measured the abundance of miR156/miR157 and their SPL targets in successive leaf primordia, and characterized the effect of variation in the abundance of miR156/miR157 on leaf morphology and the abundance of SPL transcripts and SPL proteins. miR156/miR157 are present at very high levels in the first two rosette leaves, where they act as buffers to stabilize leaf identity. They are present at lower and steadily declining levels in subsequent leaves, where they act to modulate leaf morphogenesis. In these later-formed leaves, a small decrease in the abundance of miR156/miR157 produces a disproportionately large increase in SPL activity, primarily as a result of the increased translation of SPL transcripts. Our results provide a new view of vegetative phase change in Arabidopsis and the mechanism by which miR156 and miR157 regulate this process.
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