Plant-thickening mechanisms revealed

First author: Sebastian Wolf; Affiliations: Heidelberg University (海德堡大学): Heidelberg, Germany

Corresponding author: Jan U. Lohmann

When plants evolved a vascular system containing cells that facilitate the transport of water and nutrients, this not only allowed them to conquer land, but also provided the structural stability that enabled them to increase dramatically in stature, bulk and complexity. The cells that give rise to vascular tissue are specified in the embryo, but in many flowering plants they undergo substantial rounds of proliferation only during post-embryonic development, in a process that drives radial growth and expands the circumference of roots and shoots. This radial growth depends on the division of stem cells located in an inner cylindrical layer of cells called the cambium, which gives rise to wood and the woody fibre used for textiles, called bast.

植物演化出维管系统用来转运水分和营养物质，这不仅使得它们具备了征服陆地的条件，而且还为其株高、体积及复杂程度的变化提供了稳定的结构基础。控制维管组织的细胞在胚胎时期就已经形成，但在许多开花植物中，这些细胞仅在胚后期发育经历多次增殖，该时期是驱动植物径向生长使得植物的根和茎增粗的时期。这种径向生长依赖于形成层干细胞的分裂，进而形成了木材和用于纺织的木质纤维，即韧皮。

It has been estimated that woody plant material (arising from cambial cells) accounts for more than half of Earth’s biomass. Yet despite the importance of the cambium, our level of understanding about cambial stem cells and their regulation lags behind our knowledge of stem cells in the plant root or shoot tips, probably because the cambium is more difficult to access, given its location in the interior of fully differentiated organs. Writing in Nature, Miyashima et al. and Smetana et al. offer insights into cambium development on the basis of studies of roots of the model plant Arabidopsis thaliana.

根据已有的报道估计林木占有地球整个生物量的一半以上。然而我们除了知道形成层在林木木材形成中非常重要以外，对于形成层干细胞及其调控机制远不及我们对于根尖和茎尖干细胞的理解，这可能是因为形成层位于完全分化的组织内部，使得我们很难对其进行研究。最近，来自芬兰赫尔辛基大学的Miyashima et al.和Smetana et al.同时在Nature上发文，通过模式植物拟南芥的根对形成层发育进行了研究。

Plant vascular tissue is comprised of water-transporting xylem cells and nutrient-transporting phloem cells, both of which are typically located in a central region of the mature root and stem. These specialized cell types can be separated by the cambium, which is home to dividing cells that drive the expansion of the xylem (which forms wood) and the phloem (which forms bast). Through an analysis of plants containing mutations in certain genes, and the use of imaging techniques to track fluorescently tagged proteins, Miyashima and colleagues reveal the mechanisms whereby the cell types generated by root-tip stem cells make up the cell layers from which the cambium will form. They show that cambial precursor cells, also known as procambium cells, are specified by a complex molecular network of plant hormones, transcription-factor proteins and microRNAs.

植物维管组织由能够运输水分的木质部细胞和运输营养的韧皮部细胞组成，这两种细胞都位于成熟的根和茎的中央区域。木质部和韧皮部这两种不同的细胞类型被形成层分隔开，形成层细胞向内分化形成木质部，向外分化形成韧皮部。通过对某些基因的突变体分析，以及利用图像技术追踪荧光标记蛋白，Miyashima和同事揭示了根尖干细胞产生的细胞类型组成了将来会形成形成层的细胞层。Miyashima的研究显示形成层前细胞，也叫原形成层细胞是由植物激素、转录因子和microRNA组成的一个复杂的分子网络所决定的。

Miyashima et al. report that, during an initial growth phase that precedes radial expansion, certain phloem cells at the periphery of the vascular tissue act as ‘organizers’ — cells that promote the division of nearby cells; in this case, the procambial cells. Miyashima and colleagues show that a type of developing phloem cell called a protophloem-sieve-element precursor responds to the hormone cytokinin by expressing proteins of a family of transcription factors that the authors term PEAR proteins (Fig. 1). PEAR proteins were also found in the neighbouring developing procambial cells, and the authors suggest that they reached this location from protophloem-sieve-element precursors through a cell-to-cell transport mechanism.

Miyashima et al.在文章中报道了在径向生长之前的生长起始阶段，某些维管组织边缘的韧皮部细胞会发挥“组织者”细胞，即可促进临近细胞分裂的一群细胞的作用促进原形成层细胞的分裂。Miyashima和同事发现一类发育中的韧皮部细胞，即原韧皮部筛分子前体会通过表达一系列转录因子PEAR蛋白来响应细胞分裂素。PEAR蛋白同样在邻近发育中的原形成层细胞中也有表达，作者提出这些细胞中PEAR的表达是由原韧皮部筛分子前体中的PEAR通过细胞间的转运而来的。

The presence of PEAR proteins can give cells the ability to divide; however, such division competency is limited to cells at the periphery of the vascular tissue. The authors report that this is because, towards the root interior, the hormone auxin, aided by PEAR proteins, causes HD ZIP III transcription factors to accumulate, inhibiting PEAR function. This combination of mobile and non-mobile components enables a dynamic yet robust spatial patterning of cell fate, and lays down the cellular foundation for the establishment of the cambium during the initial phase of the process leading to radial growth.

PEAR蛋白的存在可以促使细胞进行分裂，然而这种细胞分裂能力受限在维管组织的边缘区域。作者认为这是因为越向根的内部，在PEAR蛋白的辅助下，生长素会导致HD ZIP III转录因子的积累，从而抑制了PEAR的功能。可移动和不可移动调控组份的组合形成了一个决定细胞命运的动态空间模式，并且在发育起始阶段建立能够作用于后期植物径向生长的形成层提供了细胞学基础。

Focusing on later stages of root thickening, Smetana and colleagues analysed how root procambial cells, which are kept in a dormant state, develop to form the actively dividing cambium; they focused particularly on how cambial stem cells arise. The authors conducted cell-lineage-tracing experiments, which revealed that only cells adjacent to the xylem can generate cambial stem cells. They also discovered that a single individual cambial stem cell can give rise to both xylem and phloem daughter cells, which resolves a nearly 150-year-old debate over whether this occurs. By producing daughter cells of distinct fates towards the interior and exterior of the cambium, respectively, cambial stem cells differ substantially from those in root and shoot tips. In the root tip, stem cells generally produce daughter cells in one direction only. In the shoot tip, cells acquire their fate depending on their relative final position after they have left the shoot-tip region.

当聚焦到根增粗的后期，Smetana和同事分析了根原形成层细胞是如何从休眠状态发育形成能够分裂的形成层；他们关注的重点是形成层干细胞是如何增加的。作者设计了一个细胞系追踪试验，结果显示只有靠近木质部一侧的细胞能够产生形成层干细胞。他们还发现单个形成层干细胞就能够形成两个木质部和韧皮部子细胞，解决了一个争论了150年之久的问题。通过向内或向外产生细胞命运完全不同的子细胞，形成层干细胞与根和茎尖的干细胞表现出完全不同的性质。在根尖中，干细胞一般只朝着单个方向产生子细胞。在茎尖中，细胞在离开了茎尖区域后依赖于它们最终的位置而获得相应的细胞命运。

Smetana and colleagues report that cambial stem cells need to receive signals from neighbouring xylem cells that are acting as organizers. The division of cambial stem cells leads to the generation of xylem and phloem daughter cells towards the root interior and periphery, respectively. This means that xylem cells acting as organizers do so only transiently, before another cell replaces them in the position adjacent to the cambial stem cell and assumes organizer function. Smetana et al. show that the cue that determines organizer function is provided by the local accumulation of auxin, which promotes the expression of HD-ZIP III transcription factors. These, in turn, maintain the organizer cells in a non-dividing state called quiescence, which is a hallmark of this type of cell.

Smetana和同事报道了形成层干细胞需要接受来自邻近木质部细胞的信号，而这些邻近形成层的木质部细胞就是所谓的“组织者”细胞。形成层干细胞向内分裂形成木质部细胞，而向外分裂则形成韧皮部细胞。这说明邻近形成层干细胞的木质部细胞仅仅在形成层分化形成一个新的木质部细胞之前暂时发挥“组织者”细胞的作用。Smetana et al.的研究显示局部的生长素通过促进HD-ZIP III转录因子的表达来决定“组织者”细胞的功能。这些反过来维持了“组织者”细胞保持不分裂的状态，即“静止”状态，这是这类细胞的一个明显的特征。

Another discovery made by Smetana and colleagues from their lineage-tracing experiments is that organizer cells seem to differentiate without dividing, whereas cambial stem cells seem to have a fairly rapid cell-division cycle. This goes against the dogma that plant and animal stem cells usually have a lower cell-division rate than do their most recently generated daughter cells (which in this case would be organizer cells). The team’s finding that a single stem cell can give rise to xylem and phloem cells is particularly intriguing, considering that the relative rates of xylem and phloem production are not uniform, and that the generation of these tissues is subject to developmental and environmental regulation.

Smetana和同事从细胞系追踪试验中的另一个发现就是“组织者”细胞好像能够不通过分裂就分化，而形成层干细胞好像细胞分裂周期相当得快。这与之前的理解相反，之前我们认为植物和动物的干细胞通常要比他们分裂产生的子细胞，在这里子细胞就是“组织者”细胞，具有更低的分裂频率。该团队对于单个干细胞可以分化形成木质部和韧皮部的发现是非常有趣的，因为木质部和韧皮部形成的速率是不同的，而且木质部和韧皮部的产生收到发育和环境的调控。

Future research should investigate what determines whether a cambial stem cell produces phloem or xylem, how the ratio between the two cell types is coordinated across all of an organ’s cambial stem cells, and how this process results in differential tissue growth. Also unresolved is whether the determination of cell fate and cell-division activity are interdependent in the developing cambium. Understanding the mechanisms underlying any such connection might lead to the development of biotechnological approaches to enhance the production of plant biomass.

未来的研究工作应该揭示到底是什么决定了形成层干细胞形成韧皮部或者木质部，而形成这两种不同细胞类型的比率又是如何协调的，而该过程又是如何决定不同组织的生长的。另外，关于发育中的形成层的细胞命运和细胞分裂活性是否相互依赖还不清楚。对着这些问题的理解将有助于将来开发增强植物生物量的生物技术方法。

The studies by Smetana, Miyashima and their respective colleagues analysed the root procambium, which originates in the embryo. By contrast, the shoot cambium is derived post-embryonically from stem cells at the top of the shoot stem. It will be exciting to discover whether there are similarities between the molecules that drive cambial development at these two different locations in the plant. Similar molecular comparisons between cambial development in A. thaliana and in woody species might reveal the key molecules that underlie radial plant growth, and provide clues about how this growth mechanism evolved. Moreover, such work could provide a definitive answer to the highly debated question of whether A. thaliana provides a good model system for studying wood formation.

Smetana、Miyashima及其各自同事的研究分析了源自胚的根原形成层。相反，茎的形成层是在胚后期起源于茎的顶部位置。研究这两个不同的形成层发育的驱动机制是否存在相似性将十分有趣。比较拟南芥和木本植物形成层发育的分子差异可能有助于揭示植物径向生长的关键分子机制，并且为植物生长机制演化的研究提供线索。此外，这类的工作可以有助于回答关于拟南芥是否可以用作研究木材形成的模式植物的争论。

通讯：Jan U. Lohmann (https://www.cos.uni-heidelberg.de/index.php/j.lohmann?l=_e)

研究方向：以拟南芥为模式植物研究植物干细胞调控机制。

doi: 10.1038/d41586-018-07880-2

Journal: Nature

Published date: 09 January, 2019