Shumin Li, Yifang Zhang, Yuling Liu, Peiyin Zhang, Xuemin Wang, Bin Chen, Li Ding, Yingxiong Nie, Fangfang Li, Zhenbing Ma, Zhensheng Kang, Hude Mao
Drought stress limits crop yield, but the molecular modulators and their mechanisms underlying the trade-off between drought resistance and crop growth and development remain elusive. Here, a Grain width and weight2 (GW2)-like RING finger E3 ligase, TaGW2, was identified as a pivotal regulator of both kernel development and drought responses in wheat (Triticum aestivum). TaGW2 overexpression enhances drought resistance but leads to yield drag under full irrigation conditions. In contrast, TaGW2 knockdown or knockout attenuates drought resistance but remarkably increases kernel size and weight. Furthermore, TaGW2 directly interacts with and ubiquitinates the type-B Arabidopsis response regulator TaARR12, promoting its degradation via the 26S proteasome. Analysis of TaARR12 overexpression and knockdown lines indicated that TaARR12 represses the drought response but does not influence grain yield in wheat. Further DNA affinity purification sequencing combined with transcriptome analysis revealed that TaARR12 down-regulates stress-responsive genes, especially group-A basic leucine zipper (bZIP) genes, resulting in impaired drought resistance. Notably, TaARR12 knockdown in the clustered regularly interspaced short palindromic repeat (CRISPR)/CRISPR-associated nuclease 9 (Cas9)-mediated tagw2 knockout mutant leads to significantly higher drought resistance and grain yield compared to wild-type plants. Collectively, these findings show that the TaGW2–TaARR12 regulatory module is essential for drought responses, providing a strategy for improving stress resistance in high-yield wheat varieties.
干旱胁迫限制了作物产量，但抗旱性与作物生长发育之间权衡的分子调控因子及其机制仍未确定。在这里，一种类似谷粒宽度和重量2（GW2）的RING指E3连接酶TaGW2被鉴定为小麦（Triticum aestivum）籽粒发育和干旱响应的关键调控因子。TaGW2 过表达可增强抗旱性，但在充分灌溉条件下会导致产量下降。相反，TaGW2 基因敲除或基因敲除会削弱抗旱性，但会显著增加籽粒的大小和重量。此外，TaGW2 与拟南芥 B 型响应调节因子 TaARR12 直接相互作用并泛素化，促进其通过 26S 蛋白酶体降解。对 TaARR12 过表达和基因敲除株系的分析表明，TaARR12 可抑制干旱响应，但不会影响小麦的籽粒产量。进一步的 DNA 亲和纯化测序结合转录组分析表明，TaARR12 下调了胁迫响应基因，尤其是 A 组碱性亮氨酸拉链（bZIP）基因，导致抗旱性受损。值得注意的是，与野生型植株相比，在聚类规则间隔短回文重复（CRISPR）/CRISPR相关核酸酶9（Cas9）介导的tagw2基因敲除突变体中敲除TaARR12可显著提高抗旱性和谷物产量。总之，这些研究结果表明，TaGW2-TaARR12调控模块对干旱响应至关重要，为提高高产小麦品种的抗逆性提供了一种策略。
{"title":"The E3 ligase TaGW2 mediates transcription factor TaARR12 degradation to promote drought resistance in wheat","authors":"Shumin Li, Yifang Zhang, Yuling Liu, Peiyin Zhang, Xuemin Wang, Bin Chen, Li Ding, Yingxiong Nie, Fangfang Li, Zhenbing Ma, Zhensheng Kang, Hude Mao","doi":"10.1093/plcell/koad307","DOIUrl":"https://doi.org/10.1093/plcell/koad307","url":null,"abstract":"Drought stress limits crop yield, but the molecular modulators and their mechanisms underlying the trade-off between drought resistance and crop growth and development remain elusive. Here, a Grain width and weight2 (GW2)-like RING finger E3 ligase, TaGW2, was identified as a pivotal regulator of both kernel development and drought responses in wheat (Triticum aestivum). TaGW2 overexpression enhances drought resistance but leads to yield drag under full irrigation conditions. In contrast, TaGW2 knockdown or knockout attenuates drought resistance but remarkably increases kernel size and weight. Furthermore, TaGW2 directly interacts with and ubiquitinates the type-B Arabidopsis response regulator TaARR12, promoting its degradation via the 26S proteasome. Analysis of TaARR12 overexpression and knockdown lines indicated that TaARR12 represses the drought response but does not influence grain yield in wheat. Further DNA affinity purification sequencing combined with transcriptome analysis revealed that TaARR12 down-regulates stress-responsive genes, especially group-A basic leucine zipper (bZIP) genes, resulting in impaired drought resistance. Notably, TaARR12 knockdown in the clustered regularly interspaced short palindromic repeat (CRISPR)/CRISPR-associated nuclease 9 (Cas9)-mediated tagw2 knockout mutant leads to significantly higher drought resistance and grain yield compared to wild-type plants. Collectively, these findings show that the TaGW2–TaARR12 regulatory module is essential for drought responses, providing a strategy for improving stress resistance in high-yield wheat varieties.","PeriodicalId":501012,"journal":{"name":"The Plant Cell","volume":null,"pages":null},"PeriodicalIF":0.0,"publicationDate":"2023-12-12","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"138571108","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":0,"RegionCategory":"","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Sharol Schmidt-Marcec, Alyssa Parish, Tetyana Smertenko, Matthew Hickey, Bernard M A G Piette, Andrei Smertenko
The plant cytokinetic microtubule array, called the phragmoplast, exhibits higher microtubule dynamics in its center (midzone) than at the periphery (distal zone). This behavior is known as the axial asymmetry. Despite being a major characteristic of the phragmoplast, little is known about regulators of this phenomenon. Here we address the role of microtubule nucleation in axial asymmetry by characterizing MACERATOR (MACET) proteins in Arabidopsis thaliana and Nicotiana benthamiana with a combination of genetic, biochemical, and live-cell imaging assays, using photo-convertible microtubule probes, and modeling. MACET paralogs accumulate at the shrinking microtubule ends and decrease the tubulin OFF rate. Loss of MACET4 and MACET5 function abrogates axial asymmetry by suppressing microtubule dynamicity in the midzone. MACET4 also narrows the microtubule nucleation angle at the phragmoplast leading edge and functions as a microtubule tethering factor for AUGMIN COMPLEX SUBUNIT 7 (AUG7). The macet4 macet5 double mutant shows diminished clustering of AUG7 in the phragmoplast distal zone. Knockout of AUG7 does not affect MACET4 localization, axial asymmetry, or microtubule nucleation angle, but increases phragmoplast length and slows down phragmoplast expansion. The mce4-1 mce5 aug7-1 triple knockout is not viable. Experimental data and modeling demonstrate that microtubule nucleation factors regulate phragmoplast architecture and axial asymmetry directly by generating new microtubules and indirectly by modulating the abundance of free tubulin.
{"title":"The microtubule nucleating factor MACERATOR tethers AUGMIN7 to microtubules and governs phragmoplast architecture","authors":"Sharol Schmidt-Marcec, Alyssa Parish, Tetyana Smertenko, Matthew Hickey, Bernard M A G Piette, Andrei Smertenko","doi":"10.1093/plcell/koad304","DOIUrl":"https://doi.org/10.1093/plcell/koad304","url":null,"abstract":"The plant cytokinetic microtubule array, called the phragmoplast, exhibits higher microtubule dynamics in its center (midzone) than at the periphery (distal zone). This behavior is known as the axial asymmetry. Despite being a major characteristic of the phragmoplast, little is known about regulators of this phenomenon. Here we address the role of microtubule nucleation in axial asymmetry by characterizing MACERATOR (MACET) proteins in Arabidopsis thaliana and Nicotiana benthamiana with a combination of genetic, biochemical, and live-cell imaging assays, using photo-convertible microtubule probes, and modeling. MACET paralogs accumulate at the shrinking microtubule ends and decrease the tubulin OFF rate. Loss of MACET4 and MACET5 function abrogates axial asymmetry by suppressing microtubule dynamicity in the midzone. MACET4 also narrows the microtubule nucleation angle at the phragmoplast leading edge and functions as a microtubule tethering factor for AUGMIN COMPLEX SUBUNIT 7 (AUG7). The macet4 macet5 double mutant shows diminished clustering of AUG7 in the phragmoplast distal zone. Knockout of AUG7 does not affect MACET4 localization, axial asymmetry, or microtubule nucleation angle, but increases phragmoplast length and slows down phragmoplast expansion. The mce4-1 mce5 aug7-1 triple knockout is not viable. Experimental data and modeling demonstrate that microtubule nucleation factors regulate phragmoplast architecture and axial asymmetry directly by generating new microtubules and indirectly by modulating the abundance of free tubulin.","PeriodicalId":501012,"journal":{"name":"The Plant Cell","volume":null,"pages":null},"PeriodicalIF":0.0,"publicationDate":"2023-12-12","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"138571251","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":0,"RegionCategory":"","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Gabriele Bradamante, Vu Hoang Nguyen, Marco Incarbone, Zohar Meir, Heinrich Bente, Mattia Donà, Nicole Lettner, Ortrun Mittelsten Scheid, Ruben Gutzat
In sexually propagating organisms, genetic and epigenetic mutations are evolutionarily relevant only if they occur in the germline and are hence transmitted to the next generation. In contrast to most animals, plants are considered to lack an early segregating germline, implying that somatic cells can contribute genetic information to progeny. Here we demonstrate that two ARGONAUTE proteins, AGO5 and AGO9, mark cells associated with sexual reproduction in Arabidopsis (Arabidopsis thaliana) throughout development. Both AGOs are loaded with dynamically changing small RNA populations derived from highly methylated, pericentromeric, long transposons. Sequencing of single stem cell nuclei revealed that many of these transposons are co-expressed within an AGO5/9 expression domain in the shoot apical meristem (SAM). Co-occurrence of transposon expression and specific AGO expression in the SAM is reminiscent of germline features in animals and supports the existence of an early segregating germline in plants. Our results open the path to investigating transposon biology and epigenome dynamics at cellular resolution in the SAM stem cell niche.
在有性繁殖的生物体中，基因突变和表观遗传变异只有在生殖系中发生并因此传递给下一代时才具有进化意义。与大多数动物不同，植物被认为缺乏早期分离的种系，这意味着体细胞可以为后代贡献遗传信息。在这里，我们证明了两个 ARGONAUTE 蛋白 AGO5 和 AGO9 在拟南芥（Arabidopsis thaliana）的整个发育过程中标记与有性生殖相关的细胞。这两个AGOs都含有动态变化的小RNA群，这些小RNA来自高度甲基化的长转座子。对单个茎细胞核的测序显示，这些转座子中有许多是在芽尖分生组织（SAM）的 AGO5/9 表达域中共同表达的。转座子表达和特异性 AGO 表达同时出现在 SAM 中让人联想到动物的种系特征，并支持植物中存在早期分离种系。我们的研究结果为研究转座子生物学和表观基因组在SAM干细胞位点的细胞分辨率动态开辟了道路。
{"title":"Two ARG ONAUTE proteins loaded with transposon-derived small RNAs are associated with the reproductive cell lineage in Arabidopsis","authors":"Gabriele Bradamante, Vu Hoang Nguyen, Marco Incarbone, Zohar Meir, Heinrich Bente, Mattia Donà, Nicole Lettner, Ortrun Mittelsten Scheid, Ruben Gutzat","doi":"10.1093/plcell/koad295","DOIUrl":"https://doi.org/10.1093/plcell/koad295","url":null,"abstract":"In sexually propagating organisms, genetic and epigenetic mutations are evolutionarily relevant only if they occur in the germline and are hence transmitted to the next generation. In contrast to most animals, plants are considered to lack an early segregating germline, implying that somatic cells can contribute genetic information to progeny. Here we demonstrate that two ARGONAUTE proteins, AGO5 and AGO9, mark cells associated with sexual reproduction in Arabidopsis (Arabidopsis thaliana) throughout development. Both AGOs are loaded with dynamically changing small RNA populations derived from highly methylated, pericentromeric, long transposons. Sequencing of single stem cell nuclei revealed that many of these transposons are co-expressed within an AGO5/9 expression domain in the shoot apical meristem (SAM). Co-occurrence of transposon expression and specific AGO expression in the SAM is reminiscent of germline features in animals and supports the existence of an early segregating germline in plants. Our results open the path to investigating transposon biology and epigenome dynamics at cellular resolution in the SAM stem cell niche.","PeriodicalId":501012,"journal":{"name":"The Plant Cell","volume":null,"pages":null},"PeriodicalIF":0.0,"publicationDate":"2023-12-07","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"138550632","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":0,"RegionCategory":"","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Keun Pyo Lee, Kaiwei Liu, Eun Yu Kim, Laura Medina-Puche, Haihong Dong, Minghui Di, Rahul Mohan Singh, Mengping Li, Shan Qi, Zhuoling Meng, Jungnam Cho, Heng Zhang, Rosa Lozano-Duran, Chanhong Kim
N 6-methyladenosine (m6A) is a common epitranscriptional mRNA modification in eukaryotes. Thirteen putative m6A readers, mostly annotated as EVOLUTIONARILY CONSERVED C-TERMINAL REGION (ECT) proteins, have been identified in Arabidopsis (Arabidopsis thaliana), but few have been characterized. Here, we show that the Arabidopsis m6A reader ECT1 modulates salicylic acid (SA)-mediated plant stress responses. ECT1 undergoes liquid-liquid phase separation in vitro, and its N-terminal prion-like domain is critical for forming in vivo cytosolic biomolecular condensates in response to SA or bacterial pathogens. Fluorescence-activated particle sorting coupled with quantitative PCR analyses unveiled that ECT1 sequesters SA-induced m6A modification-prone mRNAs through its conserved aromatic cage to facilitate their decay in cytosolic condensates, thereby dampening SA-mediated stress responses. Consistent with this finding, ECT1 overexpression promotes bacterial multiplication in plants. Collectively, our findings unequivocally link ECT1-associated cytosolic condensates to SA-dependent plant stress responses, advancing the current understanding of m6A readers and the SA signaling network.
{"title":"The m6A reader ECT1 drives mRNA sequestration to dampen salicylic acid–dependent stress responses in Arabidopsis","authors":"Keun Pyo Lee, Kaiwei Liu, Eun Yu Kim, Laura Medina-Puche, Haihong Dong, Minghui Di, Rahul Mohan Singh, Mengping Li, Shan Qi, Zhuoling Meng, Jungnam Cho, Heng Zhang, Rosa Lozano-Duran, Chanhong Kim","doi":"10.1093/plcell/koad300","DOIUrl":"https://doi.org/10.1093/plcell/koad300","url":null,"abstract":"N 6-methyladenosine (m6A) is a common epitranscriptional mRNA modification in eukaryotes. Thirteen putative m6A readers, mostly annotated as EVOLUTIONARILY CONSERVED C-TERMINAL REGION (ECT) proteins, have been identified in Arabidopsis (Arabidopsis thaliana), but few have been characterized. Here, we show that the Arabidopsis m6A reader ECT1 modulates salicylic acid (SA)-mediated plant stress responses. ECT1 undergoes liquid-liquid phase separation in vitro, and its N-terminal prion-like domain is critical for forming in vivo cytosolic biomolecular condensates in response to SA or bacterial pathogens. Fluorescence-activated particle sorting coupled with quantitative PCR analyses unveiled that ECT1 sequesters SA-induced m6A modification-prone mRNAs through its conserved aromatic cage to facilitate their decay in cytosolic condensates, thereby dampening SA-mediated stress responses. Consistent with this finding, ECT1 overexpression promotes bacterial multiplication in plants. Collectively, our findings unequivocally link ECT1-associated cytosolic condensates to SA-dependent plant stress responses, advancing the current understanding of m6A readers and the SA signaling network.","PeriodicalId":501012,"journal":{"name":"The Plant Cell","volume":null,"pages":null},"PeriodicalIF":0.0,"publicationDate":"2023-12-02","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"138475675","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":0,"RegionCategory":"","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Auxin plays important roles throughout plant growth and development. However, the mechanisms of auxin regulation of plant structure are poorly understood. In this study, we identified a transcription factor of the BARLEY B RECOMBINANT/BASIC PENTACYSTEINE (BBR/BPC) family in apple (Malus × domestica), MdBPC2. It was highly expressed in dwarf rootstocks and it negatively regulated auxin biosynthesis. Overexpression of MdBPC2 in apple decreased plant height, altered leaf morphology, and inhibited root system development. These phenotypes were due to reduced auxin levels and were restored reversed after exogenous IAA treatment. Silencing of MdBPC2 alone had no obvious phenotypic effect, while silencing both class I and class II BPCs in apple significantly increased auxin content in plants. Biochemical analysis demonstrated that MdBPC2 directly bound to the GAGA-rich element in the promoters of the auxin synthesis genes MdYUC2a and MdYUC6b, inhibiting their transcription and reducing auxin accumulation in MdBPC2 overexpression lines. Further studies established that MdBPC2 interacted with the polycomb group (PcG) protein LIKE HETEROCHROMATIN PROTEIN 1 (LHP1) to inhibit MdYUC2a and MdYUC6b expression via methylation of histone 3 lysine 27 (H3K27me3). Silencing MdLHP1 reversed the negative effect of MdBPC2 on auxin accumulation. Our results reveal a dwarfing mechanism in perennial woody plants involving control of auxin biosynthesis by a BPC transcription factor, suggesting its use for genetic improvement of apple rootstock.
生长素在植物生长发育过程中起着重要的作用。然而，生长素调控植物结构的机制尚不清楚。在本研究中，我们在苹果(Malus × domestica)中鉴定了一个大麦B重组/碱性五半胱氨酸(BBR/BPC)家族的转录因子MdBPC2。该基因在矮秆中高表达，负向调控生长素的合成。苹果过表达MdBPC2会降低株高，改变叶片形态，抑制根系发育。这些表型是由于生长素水平降低，并在外源IAA处理后恢复逆转。单独沉默MdBPC2没有明显的表型效应，而沉默苹果中I类和II类bpc可显著提高植株生长素含量。生化分析表明，MdBPC2直接结合生长素合成基因MdYUC2a和MdYUC6b启动子中富含ga的元件，抑制其转录，减少MdBPC2过表达系中生长素的积累。进一步的研究发现，MdBPC2通过组蛋白3赖氨酸27 (H3K27me3)的甲基化，与多梳蛋白(polycomb group, PcG)蛋白LIKE HETEROCHROMATIN protein 1 (LHP1)相互作用，抑制MdYUC2a和MdYUC6b的表达。沉默MdLHP1逆转了MdBPC2对生长素积累的负面影响。我们的研究结果揭示了多年生木本植物的矮化机制涉及BPC转录因子控制生长素的生物合成，提示其可用于苹果砧木的遗传改良。
{"title":"The transcription factor MdBPC2 alters apple growth and promotes dwarfing by regulating auxin biosynthesis","authors":"Haiyan Zhao, Shuyuan Wan, Yanni Huang, Xiaoqiang Li, Tiantian Jiao, Zhijun Zhang, Baiquan Ma, Lingcheng Zhu, Fengwang Ma, Mingjun Li","doi":"10.1093/plcell/koad297","DOIUrl":"https://doi.org/10.1093/plcell/koad297","url":null,"abstract":"Auxin plays important roles throughout plant growth and development. However, the mechanisms of auxin regulation of plant structure are poorly understood. In this study, we identified a transcription factor of the BARLEY B RECOMBINANT/BASIC PENTACYSTEINE (BBR/BPC) family in apple (Malus × domestica), MdBPC2. It was highly expressed in dwarf rootstocks and it negatively regulated auxin biosynthesis. Overexpression of MdBPC2 in apple decreased plant height, altered leaf morphology, and inhibited root system development. These phenotypes were due to reduced auxin levels and were restored reversed after exogenous IAA treatment. Silencing of MdBPC2 alone had no obvious phenotypic effect, while silencing both class I and class II BPCs in apple significantly increased auxin content in plants. Biochemical analysis demonstrated that MdBPC2 directly bound to the GAGA-rich element in the promoters of the auxin synthesis genes MdYUC2a and MdYUC6b, inhibiting their transcription and reducing auxin accumulation in MdBPC2 overexpression lines. Further studies established that MdBPC2 interacted with the polycomb group (PcG) protein LIKE HETEROCHROMATIN PROTEIN 1 (LHP1) to inhibit MdYUC2a and MdYUC6b expression via methylation of histone 3 lysine 27 (H3K27me3). Silencing MdLHP1 reversed the negative effect of MdBPC2 on auxin accumulation. Our results reveal a dwarfing mechanism in perennial woody plants involving control of auxin biosynthesis by a BPC transcription factor, suggesting its use for genetic improvement of apple rootstock.","PeriodicalId":501012,"journal":{"name":"The Plant Cell","volume":null,"pages":null},"PeriodicalIF":0.0,"publicationDate":"2023-11-29","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"138455944","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":0,"RegionCategory":"","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
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