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Current Biology:生长素调控叶片展开的分子机制

叶片是植物进行光合作用的主要器官.为了最大限度提高光合能力,高等植物的叶片进化出了具有极性(即不对称性)的扁平的形状.虽然叶片的展开对于高效光合至关重要,我们尚不了解叶片原基如何在发育过程中展开以形成扁平结构.

中国科学院遗传与发育生物学研究所焦雨铃研究组的最新研究发现植物激素生长素对于叶片原基的展开至关重要.在前期的研究中,焦雨铃研究组发现叶片原基中存在生长素浓度差异,近轴面(叶片靠近茎尖一侧,即背面)生长素浓度低,远轴面(腹面)生长素浓度高(Qi et al., 2014, PNAS 111:18769-18774).通过对生长素、生长素信号转导通路下游的响应因子进行精细成像,该研究组进一步发现生长素与下游响应因子MP仅存在部分重叠,从而在近-远轴面之间的中间区界定了高生长素信号.进而,MP可以直接激活WOX1和PRS在中间区特异的表达.WOX1和PRS是中间区形成的决定因子,是叶片向两侧展开的关键.此外,叶片远轴面特异表达的生长素通路下游响应因子ARF2、ARF3和ARF4则直接抑制WOX1和PRS在远轴面区域的表达.MP和ARF2/3/4的共同作用使WOX1和PRS在叶片中间区域特异表达,从而使叶片能够展开.上述结果阐述了叶片形成过程中,近-远轴极性通过生长素信号通路介导转换为中-边轴极性,从而使叶片展开的分子机制.该课题组最近的另一项研究从生物力学的角度解释了中间区的重要性和生长素对叶片发育的调控(Qi et al., 2017, Nature Plants 3:724-733). (来源:中国科学院遗传与发育生物学研究所 主页)

该研究成果于2017年9月22日在线发表在Current Biology杂志上(DOI:10.1016/j.cub.2017.08.042).焦雨铃研究组助理研究员关春梅为论文第一作者.美国大学生物学系的Naden T. Krogan教授和中科院遗传发育所农业资源中心的刘西岗研究员参与了研究.该研究得到了科技部973项目、国家自然科学基金和植物基因组学国家重点实验室的资助

图1. 生长素及其响应因子通过调控WOX基因表达指导叶片展开

阅读延伸:该篇论文同时在境外媒体上报道:

The vast majority of higher plants use leaves to harvest solar energy. A common feature of leaves is their flat blades. Scientists from the Institute of Genetics and Developmental Biology in Beijing have discovered that the classical phytohormone auxin enables leaf blade expansion and leaf flattening.

The flattening of leaves to form broad blades is an important adaptation that maximizes photosynthesis. However, the molecular mechanism underlying this process remains unclear. A new study led by JIAO Yuling from the Institute of Genetics and Developmental Biology of the Chinese Academy of Sciences (CAS) shows that spatial auxin signaling defines the expression of two redundant genes, WOX1 and PRS, enabling leaf blade expansion and flattening.

Following their previous report on the auxin regulation of leaf polarity patterning, the researchers further found that auxin and auxin response factors (ARFs) have limited overlaps, which refines auxin signaling in the middle domain of leaf primordium. Furthermore, they found that MP/ARF5, an ARF activator directly activates the expression of WOX1 and PRS, which promote the marginal meristem and enable leaf flattening. On the other hand, ARF repressors expressed in the abaxial (ventral) domain inhibit WOX1 and PRS expression.

"The new findings in this work explain how adaxial-abaxial (dorsal-ventral) polarity patterns the mediolateral axis and subsequent lateral expansion of leaves", said Dr. JIAO Yuling. He also mentioned that other recent research of their group described auxin regulation of leaf development at the biomechanical level. "Finding how leaves get flattened is necessary to maintain and enhance yield in cultivated plants and crops," said JIAO.

This study, titled "Spatial auxin signaling controls leaf flattening in Arabidopsis," has been published online in Current Biology.

Spatial Auxin Signaling Controls Leaf Flattening in Arabidopsis

Chunmei Guan, Binbin Wu, Ting Yu, Qingqing Wang, Naden T. Krogan, Xigang Liu, Yuling JiaoCurrent Biology

DOI:10.1016/j.cub.2017.08.042

Abstract

The flattening of leaves to form broad blades is an important adaptation that maximizes photosynthesis. However, the underlying molecular mechanism of this process remains unclear. The WUSCHEL-RELATED HOMEOBOX (WOX) genes WOX1 and PRS are expressed in the leaf marginal domain to enable leaf flattening, but the nature of WOX expression establishment remains elusive. Here we report that adaxial-expressed MONOPTEROS (MP) and abaxial-enriched auxin, together, act as positional cues for patterning the WOX domain. MP directly binds to the WOX1 and PRS promoters and activates their expression. Furthermore, redundant abaxial-enriched ARF repressors suppress WOX1 and PRS expression, also through direct binding. In particular, we show ARF2 is redundantly required with ARF3 and 4 to maintain the abaxial identity. Taken together, these findings explain how adaxial-abaxial polarity patterns the mediolateral axis and subsequent lateral expansion of leaves.

导师风采:

焦雨铃研究员简介

焦雨铃,博士,研究员,博士生导师

2001年,北京大学学士;2003年,耶鲁大学硕士;2006年,耶鲁大学博士;2006年-2010年,加州理工学院从事博士后研究;2010年至今,遗传与发育生物学研究所任研究员.焦雨铃博士2005年获国家优秀自费留学生奖;2006年获耶鲁大学John Spangler Nicholas杰出生物博士毕业生奖;2011年入选中国科学院"百人计划",并在终期评估中获得优秀;2013年获国家自然科学基金委员会"优秀青年基金"资助;2015年入选中央组织部"万人计划"青年拔尖人才。

本实验室综合转录组分析、活体成像、及分子遗传学等方法,研究植物干细胞的调控与形态建成。

研究领域:

1. 茎尖干细胞与侧生器官的相互调控:茎尖分生组织具有干细胞,能够不断产生叶片、花等侧生器官.茎尖分生组织与其形成的侧生器官之间也存在着相互调控:侧生器官反馈抑制分生组织干细胞团的大小;干细胞产生信号(称为Sussex信号)调控侧生器官叶片的不对称性发育.我们的研究表明植物激素生长素的极性运输介导分生组织与叶片间的信息传递和相互调控.我们的研究还试图解答生长素的不对称分布如何导致叶片的不对称性产生.

2. 干细胞团的重建:侧生器官叶片的基部(叶腋处)能够形成新的干细胞团和分生组织,称为侧生分生组织.侧生分生组织产生侧芽,使植物能够产生分枝.开花后侧生分生组织形成花序分枝.因此,侧生分生组织的活性是决定小麦等作物关键农艺性状穗数、穗粒数的重要因素.本实验室通过活体成像、转录谱分析、以及遗传分析研究侧生分生组织发生的调控机制.特别值得一提的是,本实验室发展了高通量分析单类细胞转录谱的技术.以大量细胞特异转录谱为基础并结合高通量蛋白-DNA互作数据,我们通过重建分生组织与叶片原基分化过程的转录调控网络来系统解析这些发育过程。

代表性论文

(完整论文列表)

1. Shi, B., Zhang, C., Tian, C., Wang, J., Wang, Q., Xu, T., Xu, Y., Ohno, C., Sablowski, R., Heisler, M.G., Theres, K., Wang, Y. and Jiao, Y. (2016) Two-step regulation of a meristematic cell population acting in shoot branching in Arabidopsis. PLoS Genet. 12: e1006168.

2. Yu, H., Tian, C., Yu, Y. and Jiao, Y. (2016) Tranome survey of the contribution of alternative splicing to proteome diversity in Arabidopsis thaliana. Mol. Plant 9: 749-752.

3. Qi, J., Wang, Y., Yu, T., Cunha, A., Wu, B., Vernoux, T., Meyerowitz, E.M. and Jiao, Y. (2014) Auxin depletion from leaf primordia contributes to organ patterning. Proc. Natl Acad. Sci. USA 111: 18769-18774.

Highlighted with a Research Highlight article in Sci China Life Sci 58: 315-3164. Tian, C., Zhang, X., He, J., Yu, H., Wang, Y., Shi, B., Han, Y., Wang, G., Feng, X., Zhang, C., Wang, J., Qi, J., Yu, R. and Jiao, Y. (2014) An organ boundary-enriched gene regulatory network uncovers regulatory hierarchies underlying axillary meristem initiation. Mol. Syst. Biol. 10: 755.

5. Wang, Y., Wang, J., Shi, B., Yu, T., Qi, J., Meyerowitz, E.M. and Jiao, Y. (2014) The stem cell niche in leaf axils is established by auxin and cytokinin in Arabidopsis. Plant Cell, 26: 2055-2067.

Highlighted with an In Brief article in Plant Cell 26: 1836Selected for F1000 Prime

6. Han, Y., Zhang, C., Yang, H. and Jiao, Y. (2014) Cytokinin pathway mediates APETALA1 function in the establishment of determinate floral meristem in Arabidopsis. Proc. Natl Acad. Sci. USA, 111: 6840-6845.

7. Jiao, Y. and Meyerowitz, E.M. (2010) Cell-type specific analysis of translating RNAs in developing flowers reveals new levels of control. Mol. Syst. Biol. 6: 419.

8. Sugimoto, K., Jiao, Y. and Meyerowitz, E.M. (2010) Arabidopsis regeneration from multiple tissues occurs via a root development pathway. Dev. Cell 18: 463-471. Selected for F1000 Prime

9. Jiao, Y., Tausta, S.L., Gandotra, N., Sun, N., Liu, T., Clay, N.K., Ceserani, T., Chen, M., Ma, L., Holford, M., Zhang, H.-y., Zhao, H., Deng, X.-W. and Nelson, T. (2009) A tranome atlas of rice cell types uncovers cellular, functional and developmental hierarchies. Nat. Genet. 41: 258-263.

Selected for F1000 Prime

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