Functions and signaling mechanisms of a non-proteinogenic amino acid ACC: the case for a novel plant hormone

非蛋白氨基酸 ACC 的功能和信号机制：新型植物激素的案例

• 批准号: 1714993
• 负责人: Caren Chang
• 金额: $ 116.47万
• 依托单位: University of Maryland, College Park
• 依托单位国家: 美国
• 项目类别: Standard Grant
• 财政年份: 2017
• 资助国家: 美国
• 起止时间: 2017-07-01 至 2023-06-30
• 项目状态: 已结题
• 来源: https://www.nsf.gov/awardsearch/showAward?AWD_ID=1714993&HistoricalAwards=false
• 关键词: Functions; signaling; mechanisms; non; proteinogenic

Plants produce hormones such as ethylene that collectively control essentially all aspects of plant biology. This project advances a new hypothesis that a small molecule, which plants use to make ethylene, functions itself as a novel plant hormone that impacts plant growth and development, and further investigates how the hormone functions at the molecular level throughout the evolutionary breadth of plants. The project has the potential to transform the plant hormone field by altering existing dogma, by requiring the reevaluation of several decades of ethylene literature and by impacting how future ethylene experiments are carried out. The knowledge gained from this project could contribute to future strategies for modifying crop plants for the benefit of society. The project broadens participation of underrepresented students by providing two to three student internships per year in the lab of the principal investigator. The internships involve partnerships with Howard University (an Historically Black College or University) and Eleanor Roosevelt High School (a local public school in which over 70% of the students are underrepresented minorities). The interns carry out aspects of the project while receiving valuable training in scientific methods, data analysis and communication. The project also provides training and career preparation for two postdoctoral scientists, two graduate students and two University of Maryland undergraduates. To further broaden participation, the principal investigator co-teaches summer research workshops for Howard University undergraduates. The well-known ethylene precursor in the ethylene biosynthesis pathway is 1-aminocyclopropane-1-carboxylic acid (ACC), a non-proteinogenic amino acid. Compelling new data suggest that ACC itself may be an important signaling molecule that evolutionarily predated the ability of higher land plants to efficiently convert ACC to ethylene. In particular, ACC inhibits cellular differentiation and growth in the liverwort Marchantia polymorpha. This project tests the hypothesis that ACC is a novel plant hormone through analyses of ACC function, including an investigation of ACC signaling mechanisms. Insight into ACC function is provided by studies of ACC synthesis mutants and ACC responses in Marchantia, and in evolutionarily relevant species in the plant lineage (Chlamydomonas reinhardtii, Spirogyra pratensis, Physcomitrella patens and Arabidopsis thaliana), thus addressing the conservation of ACC function, while taking advantage of lower gene copy number in basal plants. In Arabidopsis, preliminary findings indicate that ACC can induce pollen tube growth concomitant with Ca2+ influx and can stimulate primary root growth. ACC activates Ca2+ currents in Arabidopsis root protoplasts, and notably, this activation is dependent on glutamate receptor-like (GLR) ionotropic channels. The project tests the hypothesis that ACC is a GLR ligand using a combination of molecular genetics, patch-clamping, ion-specific vibrating probes and live imaging of Ca2+. Genetic evidence is sought based on phenotypic comparisons of glr mutants and ACC synthesis mutants in the range of plant species. The activation of GLRs by ACC, leading to the regulation of Ca2+ signaling in pollen tube growth and/or root growth, would be a breakthrough in understanding mechanisms of ACC signaling, as well as GLR signaling, and would represent a ligand-operated system of Ca2+ regulation for which no consensual system currently exists in plants. The striking ACC response uncovered in Marchantia provides for a genetic screen for ACC signaling mutants, followed by gene cloning based on T-DNA tagging or whole genome sequencing.

植物产生乙烯等激素，这些激素基本上共同控制植物生物学的所有方面。该项目提出了一个新的假设，即植物用来制造乙烯的小分子本身作为一种影响植物生长和发育的新型植物激素发挥作用，并进一步研究了这种激素在整个植物进化过程中如何在分子水平上发挥作用。该项目有可能通过改变现有的教条、要求重新评估数十年的乙烯文献以及影响未来乙烯实验的进行方式来改变植物激素领域。从该项目中获得的知识可以有助于未来改造农作物以造福社会的战略。该项目每年在首席研究员的实验室提供两到三个学生实习机会，扩大了代表性不足的学生的参与。实习涉及与霍华德大学（一所历史悠久的黑人学院或大学）和埃莉诺罗斯福高中（一所当地公立学校，其中 70% 以上的学生是少数族裔）的合作伙伴关系。实习生在执行该项目的各个方面的同时，还接受了科学方法、数据分析和沟通方面的宝贵培训。该项目还为两名博士后科学家、两名研究生和两名马里兰大学本科生提供培训和职业准备。为了进一步扩大参与范围，首席研究员为霍华德大学本科生共同教授夏季研究研讨会。乙烯生物合成途径中众所周知的乙烯前体是 1-氨基环丙烷-1-羧酸 (ACC)，一种非蛋白氨基酸。令人信服的新数据表明，ACC 本身可能是一种重要的信号分子，其进化早于高等陆地植物有效地将 ACC 转化为乙烯的能力。特别是，ACC 抑制地钱地钱的细胞分化和生长。该项目通过分析 ACC 功能（包括研究 ACC 信号机制）来检验 ACC 是一种新型植物激素的假设。通过对地钱属以及植物谱系中进化相关物种（莱茵衣藻、草地水绵、小立碗藓和拟南芥）的 ACC 合成突变体和 ACC 反应的研究，深入了解 ACC 功能，从而解决了 ACC 功能的保护问题，同时利用基础植物中较低的基因拷贝数。在拟南芥中，初步研究结果表明，ACC 可以诱导花粉管生长并伴随 Ca2+ 流入，并可以刺激初生根生长。 ACC 激活拟南芥根原生质体中的 Ca2+ 电流，值得注意的是，这种激活依赖于谷氨酸受体样 (GLR) 离子通道。该项目结合使用分子遗传学、膜片钳、离子特异性振动探针和 Ca2+ 实时成像，测试了 ACC 是 GLR 配体这一假设。根据植物物种范围内 glr 突变体和 ACC 合成突变体的表型比较来寻找遗传证据。 ACC 激活 GLR，导致花粉管生长和/或根生长中 Ca2+ 信号传导的调节，这将是理解 ACC 信号传导和 GLR 信号传导机制的突破，并且将代表一种配体操纵的 Ca2+ 调节系统，目前植物中尚不存在共识系统。在地钱属中发现的引人注目的 ACC 反应为 ACC 信号突变体提供了遗传筛选，然后基于 T-DNA 标签或全基因组测序进行基因克隆。

项目成果

A transporter of 1‐aminocyclopropane‐1‐carboxylic acid affects thallus growth and fertility in Marchantia polymorpha

1-氨基环丙烷-1-羧酸转运蛋白对地钱菌体生长和育性的影响

• DOI: 10.1111/nph.18510
• 发表时间: 2022
• 期刊: New Phytologist
• 影响因子: 9.4
• 作者: Li, Dongdong;Dierschke, Tom;Roden, Stijn;Chen, Kunsong;Bowman, John L.;Chang, Caren;Van de Poel, Bram
• 通讯作者: Van de Poel, Bram

The Chara Genome: Secondary Complexity and Implications for Plant Terrestrialization

• DOI: 10.1016/j.cell.2018.06.033
• 发表时间: 2018-07-12
• 期刊: CELL
• 影响因子: 64.5
• 作者: Nishiyama, Tomoaki;Sakayama, Hidetoshi;Rensing, Stefan A.
• 通讯作者: Rensing, Stefan A.

Ethylene-independent signaling by the ethylene precursor ACC in Arabidopsis ovular pollen tube attraction

• DOI: 10.1038/s41467-020-17819-9
• 发表时间: 2020-08-14
• 期刊: NATURE COMMUNICATIONS
• 影响因子: 16.6
• 作者: Mou, Wangshu;Kao, Yun-Ting;Chang, Caren
• 通讯作者: Chang, Caren

Ethylene-independent functions of the ethylene precursor ACC in Marchantia polymorpha

• DOI: 10.1038/s41477-020-00784-y
• 发表时间: 2020-10-26
• 期刊: NATURE PLANTS
• 影响因子: 18
• 作者: Li, Dongdong;Flores-Sandoval, Eduardo;Chang, Caren
• 通讯作者: Chang, Caren

Is losing ethylene a losing game?

失去乙烯是一场失败的游戏吗？

• DOI: 10.1016/j.molp.2022.03.005
• 发表时间: 2022
• 期刊: Molecular Plant
• 影响因子: 27.5
• 作者: Van de Poel, Bram;Chang, Caren
• 通讯作者: Chang, Caren