Mobile PEAR transcription factors integrate positional cues to prime cambial growth

First author: Shunsuke Miyashima; Affiliations: University of Helsinki (赫尔辛基大学): Helsinki, Finland

Corresponding author: Ykä Helariutta 

Apical growth in plants initiates upon seed germination, whereas radial growth is primed only during early ontogenesis in procambium cells and activated later by the vascular cambium. Although it is not known how radial growth is organized and regulated in plants, this system resembles the developmental competence observed in some animal systems, in which pre-existing patterns of developmental potential are established early on. Here we show that in Arabidopsis the initiation of radial growth occurs around early protophloem-sieve-element (原韧皮部筛分子) cell files of the root procambial tissue. In this domain, cytokinin signalling promotes the expression of a pair of mobile transcription factors—PHLOEM EARLY DOF 1 (PEAR1) and PHLOEM EARLY DOF 2 (PEAR2)—and their four homologues (DOF6, TMO6, OBP2 and HCA2), which we collectively name PEAR proteins. The PEAR proteins form a short-range concentration gradient that peaks at protophloem sieve elements, and activates gene expression that promotes radial growth. The expression and function of PEAR proteins are antagonized by the HD-ZIP III proteins, well-known polarity transcription factors—the expression of which is concentrated in the more-internal domain of radially non-dividing procambial cells by the function of auxin, and mobile miR165 and miR166 microRNAs. The PEAR proteins locally promote transcription of their inhibitory HD-ZIP III genes, and thereby establish a negative-feedback loop that forms a robust boundary that demarks the zone of cell division. Taken together, our data establish that during root procambial development there exists a network in which a module that links PEAR and HD-ZIP III transcription factors integrates spatial information of the hormonal domains and miRNA gradients to provide adjacent zones of dividing and more-quiescent cells, which forms a foundation for further radial growth.

植物的顶端生长在种子萌发时就已经开始，而径向生长在原形成层细胞早期发育时才起始，而后由围观形成层所激活。尽管，目前还不清楚植物的径向生长是如何起始和调控的，但该系统的特征在于发育模式在很早的时候就已经建立，这种发育模式类似于在某些动物系统中所观察到的发育能力。本文研究显示拟南芥径向生长的起始发生于根原形成层组织的早期原韧皮部筛分子细胞。该区域的细胞分裂素信号促进了一对可移动的转录因子PEAR1和PEAR2以及它们四个同源基因DOF6、TMO6、OBP2和HCA2的表达，本文作者将这些蛋白都命名为PEAR蛋白。PEAR蛋白会形成一个小范围的浓度梯度，峰值出现在原韧皮部筛分子，激活能够促进植物径向生长的基因的表达。PEAR蛋白的表达和功能受到HD-ZIP III蛋白的拮抗，这是一类总所周知的极性转录因子，受到生长素、miR165和miR166的影响主要在径向不分裂的原形成层细胞的内侧表达。PEAR蛋白能够促进其抑制基因HD-ZIP III基因的表达，因此建立了一个负反馈调节通路，进而形成了一个细胞分裂区域的边界。综上，本文的研究说明在根原形成层发育时存在一个调控网络，该调控网络中的一个模块由PEAR与HD-ZIP III转录因子构成，通过整合激素和miRNA梯度的空间信息以确保分裂和静止细胞的分界线，这为植物后续的径向生长提供了基础。

通讯：Ykä Helariutta (http://www.biocenter.helsinki.fi/bi/Helariutta/yka.htm)

个人简介：1990年，芬兰赫尔辛基大学，遗传学硕士；1995年，芬兰赫尔辛基大学，博士。

研究方向：植物的木材形成。

doi: https://doi.org/10.1038/s41586-018-0839-y

Journal: Nature

Published date: 09 January, 2019