Pub Date : 2024-07-01Epub Date: 2024-06-01DOI: 10.1016/j.molp.2024.05.011
Shen Zhang, Devasantosh Mohanty, Adnan Muzaffar, Min Ni
Spatiotemporal regulation of gene expression by polycomb repressive complex 2 (PRC2) is critical for animal and plant development. The Arabidopsis fertilization independent seed (FIS)-PRC2 complex functions specifically during plant reproduction from gametogenesis to seed development. After a double fertilization event, triploid endosperm proliferates early, followed by the growth of a diploid embryo, which replaces the endosperm in Arabidopsis and many dicots. Key genes critical for endosperm proliferation such as IKU2 and MINI3 are activated after fertilization. Here we report that two MADS-box AGAMOUS-LIKE (AGL) proteins associate with the key endosperm proliferation loci and recruit the FIS-PRC2 repressive complex at 4-5 days after pollination (DAP). Interestingly, AGL9 and AGL15 only accumulate toward the end of endosperm proliferation at 4-5 DAP and promote the deposition of H3K27me3 marks at key endosperm proliferation loci. Disruption of AGL9 and AGL15 or overexpression of AGL9 or AGL15 significantly influence endosperm proliferation and cellularization. Genome-wide analysis with cleavage Under Targets and tagmentation (CUT&Tag) sequencing and RNA sequencing revealed the landscape of endosperm H3K27me3 marks and gene expression profiles in Col-0 and agl9 agl15. CUT&Tag qPCR also demonstrated the occupancy of the two MADS-box proteins and FIS-PRC2 on a few representative target loci. Our studies suggest that MADS-box proteins could potentially recruit PRC2 to regulate many other developmental processes in plants or even in fungi and animals.
{"title":"Two MADS-box proteins, AGL9 and AGL15, recruit the FIS-PRC2 complex to trigger the phase transition from endosperm proliferation to embryo development in Arabidopsis.","authors":"Shen Zhang, Devasantosh Mohanty, Adnan Muzaffar, Min Ni","doi":"10.1016/j.molp.2024.05.011","DOIUrl":"10.1016/j.molp.2024.05.011","url":null,"abstract":"<p><p>Spatiotemporal regulation of gene expression by polycomb repressive complex 2 (PRC2) is critical for animal and plant development. The Arabidopsis fertilization independent seed (FIS)-PRC2 complex functions specifically during plant reproduction from gametogenesis to seed development. After a double fertilization event, triploid endosperm proliferates early, followed by the growth of a diploid embryo, which replaces the endosperm in Arabidopsis and many dicots. Key genes critical for endosperm proliferation such as IKU2 and MINI3 are activated after fertilization. Here we report that two MADS-box AGAMOUS-LIKE (AGL) proteins associate with the key endosperm proliferation loci and recruit the FIS-PRC2 repressive complex at 4-5 days after pollination (DAP). Interestingly, AGL9 and AGL15 only accumulate toward the end of endosperm proliferation at 4-5 DAP and promote the deposition of H3K27me3 marks at key endosperm proliferation loci. Disruption of AGL9 and AGL15 or overexpression of AGL9 or AGL15 significantly influence endosperm proliferation and cellularization. Genome-wide analysis with cleavage Under Targets and tagmentation (CUT&Tag) sequencing and RNA sequencing revealed the landscape of endosperm H3K27me3 marks and gene expression profiles in Col-0 and agl9 agl15. CUT&Tag qPCR also demonstrated the occupancy of the two MADS-box proteins and FIS-PRC2 on a few representative target loci. Our studies suggest that MADS-box proteins could potentially recruit PRC2 to regulate many other developmental processes in plants or even in fungi and animals.</p>","PeriodicalId":19012,"journal":{"name":"Molecular Plant","volume":" ","pages":"1110-1128"},"PeriodicalIF":17.1,"publicationDate":"2024-07-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141200142","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Pub Date : 2024-07-01Epub Date: 2024-06-04DOI: 10.1016/j.molp.2024.05.013
Chunmei Jiang, Jinqiu Fu, Fujun Li, Kai Xia, Shengchun Li, Ling Chang, Ralph Bock, Jiang Zhang
{"title":"Plastid engineering with an efficient RNAi delivery system based on bacteriophage MS2 virus-like particles enhances plant resistance to cotton bollworm.","authors":"Chunmei Jiang, Jinqiu Fu, Fujun Li, Kai Xia, Shengchun Li, Ling Chang, Ralph Bock, Jiang Zhang","doi":"10.1016/j.molp.2024.05.013","DOIUrl":"10.1016/j.molp.2024.05.013","url":null,"abstract":"","PeriodicalId":19012,"journal":{"name":"Molecular Plant","volume":" ","pages":"987-989"},"PeriodicalIF":17.1,"publicationDate":"2024-07-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141248111","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Pub Date : 2024-07-01Epub Date: 2024-06-03DOI: 10.1016/j.molp.2024.05.004
Esther Riemer, Danye Qiu, Debabrata Laha, Robert K Harmel, Philipp Gaugler, Verena Gaugler, Michael Frei, Mohammad-Reza Hajirezaei, Nargis Parvin Laha, Lukas Krusenbaum, Robin Schneider, Adolfo Saiardi, Dorothea Fiedler, Henning J Jessen, Gabriel Schaaf, Ricardo F H Giehl
{"title":"ITPK1 is an InsP<sub>6</sub>/ADP phosphotransferase that controls phosphate signaling in Arabidopsis.","authors":"Esther Riemer, Danye Qiu, Debabrata Laha, Robert K Harmel, Philipp Gaugler, Verena Gaugler, Michael Frei, Mohammad-Reza Hajirezaei, Nargis Parvin Laha, Lukas Krusenbaum, Robin Schneider, Adolfo Saiardi, Dorothea Fiedler, Henning J Jessen, Gabriel Schaaf, Ricardo F H Giehl","doi":"10.1016/j.molp.2024.05.004","DOIUrl":"10.1016/j.molp.2024.05.004","url":null,"abstract":"","PeriodicalId":19012,"journal":{"name":"Molecular Plant","volume":" ","pages":"1151-1157"},"PeriodicalIF":17.1,"publicationDate":"2024-07-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11239801/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141248092","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Pub Date : 2024-07-01Epub Date: 2024-06-03DOI: 10.1016/j.molp.2024.05.012
Paula Berman, Luis Alejandro de Haro, Ana-Rita Cavaco, Sayantan Panda, Younghui Dong, Nikolay Kuzmich, Gabriel Lichtenstein, Yoav Peleg, Hila Harat, Adam Jozwiak, Jianghua Cai, Uwe Heinig, Sagit Meir, Ilana Rogachev, Asaph Aharoni
Mescaline, among the earliest identified natural hallucinogens, holds great potential in psychotherapy treatment. Nonetheless, despite the existence of a postulated biosynthetic pathway for more than half a century, the specific enzymes involved in this process are yet to be identified. In this study, we investigated the cactus Lophophora williamsii (Peyote), the largest known natural producer of the phenethylamine mescaline. We employed a multi-faceted approach, combining de novo whole-genome and transcriptome sequencing with comprehensive chemical profiling, enzymatic assays, molecular modeling, and pathway engineering for pathway elucidation. We identified four groups of enzymes responsible for the six catalytic steps in the mescaline biosynthetic pathway, and an N-methyltransferase enzyme that N-methylates all phenethylamine intermediates, likely modulating mescaline levels in Peyote. Finally, we reconstructed the mescaline biosynthetic pathway in both Nicotiana benthamiana plants and yeast cells, providing novel insights into several challenges hindering complete heterologous mescaline production. Taken together, our study opens up avenues for exploration of sustainable production approaches and responsible utilization of mescaline, safeguarding this valuable natural resource for future generations.
{"title":"The biosynthetic pathway of the hallucinogen mescaline and its heterologous reconstruction.","authors":"Paula Berman, Luis Alejandro de Haro, Ana-Rita Cavaco, Sayantan Panda, Younghui Dong, Nikolay Kuzmich, Gabriel Lichtenstein, Yoav Peleg, Hila Harat, Adam Jozwiak, Jianghua Cai, Uwe Heinig, Sagit Meir, Ilana Rogachev, Asaph Aharoni","doi":"10.1016/j.molp.2024.05.012","DOIUrl":"10.1016/j.molp.2024.05.012","url":null,"abstract":"<p><p>Mescaline, among the earliest identified natural hallucinogens, holds great potential in psychotherapy treatment. Nonetheless, despite the existence of a postulated biosynthetic pathway for more than half a century, the specific enzymes involved in this process are yet to be identified. In this study, we investigated the cactus Lophophora williamsii (Peyote), the largest known natural producer of the phenethylamine mescaline. We employed a multi-faceted approach, combining de novo whole-genome and transcriptome sequencing with comprehensive chemical profiling, enzymatic assays, molecular modeling, and pathway engineering for pathway elucidation. We identified four groups of enzymes responsible for the six catalytic steps in the mescaline biosynthetic pathway, and an N-methyltransferase enzyme that N-methylates all phenethylamine intermediates, likely modulating mescaline levels in Peyote. Finally, we reconstructed the mescaline biosynthetic pathway in both Nicotiana benthamiana plants and yeast cells, providing novel insights into several challenges hindering complete heterologous mescaline production. Taken together, our study opens up avenues for exploration of sustainable production approaches and responsible utilization of mescaline, safeguarding this valuable natural resource for future generations.</p>","PeriodicalId":19012,"journal":{"name":"Molecular Plant","volume":" ","pages":"1129-1150"},"PeriodicalIF":17.1,"publicationDate":"2024-07-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141248118","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Pub Date : 2024-07-01Epub Date: 2024-06-13DOI: 10.1016/j.molp.2024.06.005
Yanzhi Qu, Alisdair R Fernie, Jie Liu, Jianbing Yan
Doubled haploid (DH) technology and synthetic apomixis approaches can considerably shorten breeding cycles and enhance breeding efficiency. Compared with traditional breeding methods, DH technology offers the advantage of rapidly generating inbred lines, while synthetic apomixis can effectively fix hybrid vigor. In this review, we focus on (i) recent advances in identifying and characterizing genes responsible for haploid induction (HI), (ii) the molecular mechanisms of HI, (iii) spontaneous haploid genome doubling, and (iv) crop synthetic apomixis. We also discuss the challenges and potential solutions for future crop breeding programs utilizing DH technology and synthetic apomixis. Finally, we provide our perspectives about how to integrate DH and synthetic apomixis for precision breeding and de novo domestication.
{"title":"Doubled haploid technology and synthetic apomixis: Recent advances and applications in future crop breeding.","authors":"Yanzhi Qu, Alisdair R Fernie, Jie Liu, Jianbing Yan","doi":"10.1016/j.molp.2024.06.005","DOIUrl":"10.1016/j.molp.2024.06.005","url":null,"abstract":"<p><p>Doubled haploid (DH) technology and synthetic apomixis approaches can considerably shorten breeding cycles and enhance breeding efficiency. Compared with traditional breeding methods, DH technology offers the advantage of rapidly generating inbred lines, while synthetic apomixis can effectively fix hybrid vigor. In this review, we focus on (i) recent advances in identifying and characterizing genes responsible for haploid induction (HI), (ii) the molecular mechanisms of HI, (iii) spontaneous haploid genome doubling, and (iv) crop synthetic apomixis. We also discuss the challenges and potential solutions for future crop breeding programs utilizing DH technology and synthetic apomixis. Finally, we provide our perspectives about how to integrate DH and synthetic apomixis for precision breeding and de novo domestication.</p>","PeriodicalId":19012,"journal":{"name":"Molecular Plant","volume":" ","pages":"1005-1018"},"PeriodicalIF":17.1,"publicationDate":"2024-07-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141321276","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Pub Date : 2024-07-01Epub Date: 2024-05-24DOI: 10.1016/j.molp.2024.05.006
Zhaoheng Zhang, Dan Liu, Binyong Li, Wenxi Wang, Jize Zhang, Mingming Xin, Zhaorong Hu, Jie Liu, Jinkun Du, Huiru Peng, Chenyang Hao, Xueyong Zhang, Zhongfu Ni, Qixin Sun, Weilong Guo, Yingyin Yao
Wheat is a staple food for more than 35% of the world's population, with wheat flour used to make hundreds of baked goods. Superior end-use quality is a major breeding target; however, improving it is especially time-consuming and expensive. Furthermore, genes encoding seed-storage proteins (SSPs) form multi-gene families and are repetitive, with gaps commonplace in several genome assemblies. To overcome these barriers and efficiently identify superior wheat SSP alleles, we developed "PanSK" (Pan-SSP k-mer) for genotype-to-phenotype prediction based on an SSP-based pangenome resource. PanSK uses 29-mer sequences that represent each SSP gene at the pangenomic level to reveal untapped diversity across landraces and modern cultivars. Genome-wide association studies with k-mers identified 23 SSP genes associated with end-use quality that represent novel targets for improvement. We evaluated the effect of rye secalin genes on end-use quality and found that removal of ω-secalins from 1BL/1RS wheat translocation lines is associated with enhanced end-use quality. Finally, using machine-learning-based prediction inspired by PanSK, we predicted the quality phenotypes with high accuracy from genotypes alone. This study provides an effective approach for genome design based on SSP genes, enabling the breeding of wheat varieties with superior processing capabilities and improved end-use quality.
{"title":"A k-mer-based pangenome approach for cataloging seed-storage-protein genes in wheat to facilitate genotype-to-phenotype prediction and improvement of end-use quality.","authors":"Zhaoheng Zhang, Dan Liu, Binyong Li, Wenxi Wang, Jize Zhang, Mingming Xin, Zhaorong Hu, Jie Liu, Jinkun Du, Huiru Peng, Chenyang Hao, Xueyong Zhang, Zhongfu Ni, Qixin Sun, Weilong Guo, Yingyin Yao","doi":"10.1016/j.molp.2024.05.006","DOIUrl":"10.1016/j.molp.2024.05.006","url":null,"abstract":"<p><p>Wheat is a staple food for more than 35% of the world's population, with wheat flour used to make hundreds of baked goods. Superior end-use quality is a major breeding target; however, improving it is especially time-consuming and expensive. Furthermore, genes encoding seed-storage proteins (SSPs) form multi-gene families and are repetitive, with gaps commonplace in several genome assemblies. To overcome these barriers and efficiently identify superior wheat SSP alleles, we developed \"PanSK\" (Pan-SSP k-mer) for genotype-to-phenotype prediction based on an SSP-based pangenome resource. PanSK uses 29-mer sequences that represent each SSP gene at the pangenomic level to reveal untapped diversity across landraces and modern cultivars. Genome-wide association studies with k-mers identified 23 SSP genes associated with end-use quality that represent novel targets for improvement. We evaluated the effect of rye secalin genes on end-use quality and found that removal of ω-secalins from 1BL/1RS wheat translocation lines is associated with enhanced end-use quality. Finally, using machine-learning-based prediction inspired by PanSK, we predicted the quality phenotypes with high accuracy from genotypes alone. This study provides an effective approach for genome design based on SSP genes, enabling the breeding of wheat varieties with superior processing capabilities and improved end-use quality.</p>","PeriodicalId":19012,"journal":{"name":"Molecular Plant","volume":" ","pages":"1038-1053"},"PeriodicalIF":17.1,"publicationDate":"2024-07-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141154525","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Pub Date : 2024-07-01Epub Date: 2024-06-13DOI: 10.1016/j.molp.2024.06.007
Yonghao Sun, Liang Dong, Lu Kang, Wanshun Zhong, David Jackson, Fang Yang
Maize develops separate ear and tassel inflorescences with initially similar morphology but ultimately different architecture and sexuality. The detailed regulatory mechanisms underlying these changes still remain largely unclear. In this study, through analyzing the time-course meristem transcriptomes and floret single-cell transcriptomes of ear and tassel, we revealed the regulatory dynamics and pathways underlying inflorescence development and sex differentiation. We identified 16 diverse gene clusters with differential spatiotemporal expression patterns and revealed biased regulation of redox, programmed cell death, and hormone signals during meristem differentiation between ear and tassel. Notably, based on their dynamic expression patterns, we revealed the roles of two RNA-binding proteins in regulating inflorescence meristem activity and axillary meristem formation. Moreover, using the transcriptional profiles of 53 910 single cells, we uncovered the cellular heterogeneity between ear and tassel florets. We found that multiple signals associated with either enhanced cell death or reduced growth are responsible for tassel pistil suppression, while part of the gibberellic acid signal may act non-cell-autonomously to regulate ear stamen arrest during sex differentiation. We further showed that the pistil-protection gene SILKLESS 1 (SK1) functions antagonistically to the known pistil-suppression genes through regulating common molecular pathways, and constructed a regulatory network for pistil-fate determination. Collectively, our study provides a deep understanding of the regulatory mechanisms underlying inflorescence development and sex differentiation in maize, laying the foundation for identifying new regulators and pathways for maize hybrid breeding and improvement.
玉米的穗花序和抽穗花序最初形态相似,但最后结构和性状却不同。这些变化背后的详细调控机制在很大程度上仍不清楚。本研究通过分析穗和缨的分生组织转录组和小花单细胞转录组,揭示了花序发育和性别分化的调控动态和途径。我们发现了16个具有不同时空表达模式的基因簇,并揭示了氧化还原、程序性细胞死亡和激素信号对穗和缨之间分生组织分化的偏向调控。特别是,根据它们的动态模式,我们揭示了两种 RNA 结合蛋白在调控花序分生组织活性和腋生分生组织形成中的作用。此外,利用 53,910 个单细胞的转录图谱,我们发现了穗小花和缨小花之间的细胞异质性。我们发现,与细胞死亡增强或生长减弱相关的多种信号是造成穗状花序雌蕊抑制的原因,而部分 GA 信号可能在性分化过程中以非细胞自主的方式调节穗状花序雄蕊的停滞。我们进一步发现,雌蕊保护基因SILKLESS 1(SK1)通过调控共同的分子通路与已知的雌蕊抑制基因起拮抗作用,并构建了雌蕊命运决定的调控模型。总之,我们的研究加深了对玉米花序发育和性别分化调控机制的理解,为确定玉米杂交育种和改良的新调控因子和途径奠定了基础。
{"title":"Progressive meristem and single-cell transcriptomes reveal the regulatory mechanisms underlying maize inflorescence development and sex differentiation.","authors":"Yonghao Sun, Liang Dong, Lu Kang, Wanshun Zhong, David Jackson, Fang Yang","doi":"10.1016/j.molp.2024.06.007","DOIUrl":"10.1016/j.molp.2024.06.007","url":null,"abstract":"<p><p>Maize develops separate ear and tassel inflorescences with initially similar morphology but ultimately different architecture and sexuality. The detailed regulatory mechanisms underlying these changes still remain largely unclear. In this study, through analyzing the time-course meristem transcriptomes and floret single-cell transcriptomes of ear and tassel, we revealed the regulatory dynamics and pathways underlying inflorescence development and sex differentiation. We identified 16 diverse gene clusters with differential spatiotemporal expression patterns and revealed biased regulation of redox, programmed cell death, and hormone signals during meristem differentiation between ear and tassel. Notably, based on their dynamic expression patterns, we revealed the roles of two RNA-binding proteins in regulating inflorescence meristem activity and axillary meristem formation. Moreover, using the transcriptional profiles of 53 910 single cells, we uncovered the cellular heterogeneity between ear and tassel florets. We found that multiple signals associated with either enhanced cell death or reduced growth are responsible for tassel pistil suppression, while part of the gibberellic acid signal may act non-cell-autonomously to regulate ear stamen arrest during sex differentiation. We further showed that the pistil-protection gene SILKLESS 1 (SK1) functions antagonistically to the known pistil-suppression genes through regulating common molecular pathways, and constructed a regulatory network for pistil-fate determination. Collectively, our study provides a deep understanding of the regulatory mechanisms underlying inflorescence development and sex differentiation in maize, laying the foundation for identifying new regulators and pathways for maize hybrid breeding and improvement.</p>","PeriodicalId":19012,"journal":{"name":"Molecular Plant","volume":" ","pages":"1019-1037"},"PeriodicalIF":17.1,"publicationDate":"2024-07-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141321277","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Pub Date : 2024-07-01Epub Date: 2024-05-27DOI: 10.1016/j.molp.2024.05.008
Francisco J Escaray, Amelia Felipo-Benavent, Cristian J Antonelli, Begoña Balaguer, Maria Pilar Lopez-Gresa, Pablo Vera
The gray mold fungus Botrytis cinerea is a necrotrophic pathogen that causes diseases in hundreds of plant species, including high-value crops. Its polyxenous nature and pathogenic success are due to its ability to perceive host signals in its favor. In this study, we found that laticifer cells of Euphorbia lathyris are a source of susceptibility factors required by B. cinerea to cause disease. Consequently, poor-in-latex (pil) mutants, which lack laticifer cells, show full resistance to this pathogen, whereas lot-of-latex mutants, which produce more laticifer cells, are hypersusceptible. These S factors are triterpenoid saponins, which are widely distributed natural products of vast structural diversity. The downregulation of laticifer-specific oxydosqualene cyclase genes, which encode the first committed step enzymes for triterpene and, therefore, saponin biosynthesis, conferred disease resistance to B. cinerea. Likewise, the Medicago truncatula lha-1 mutant, compromised in triterpenoid saponin biosynthesis, showed enhanced resistance. Interestingly, the application of different purified triterpenoid saponins pharmacologically complemented the disease-resistant phenotype of pil and hla-1 mutants and enhanced disease susceptibility in different plant species. We found that triterpenoid saponins function as plant cues that signal transcriptional reprogramming in B. cinerea, leading to a change in its growth habit and infection strategy, culminating in the abundant formation of infection cushions, the multicellular appressoria apparatus dedicated to plant penetration and biomass destruction in B. cinerea. Taken together, these results provide an explanation for how plant triterpenoid saponins function as disease susceptibility factors to promote B. cinerea pathogenicity.
灰霉病菌(Botrytis cinerea)是一种坏死性病原体,可导致数百种植物(包括高价值作物)发病。这种多腺性和致病性的成功是由于它能够感知寄主对其有利的信号。我们发现,Euphorbia lathyris 的小叶细胞是 B. cinerea 致病所需的易感因子(S)的来源。因此,缺乏鳞叶细胞的poor-in-latex(pil)突变体对这种病原体表现出完全的抗性,而产生更多鳞叶细胞的lot-of-latex(lol)突变体则易感。这些 S因子是三萜类皂苷,是分布广泛、结构多样的天然产物。下调拉蒂西弗特异性氧代喹啉环化酶(OSCs)基因(OSCs 编码三萜类生物合成的第一步酶,因此也是皂苷生物合成的第一步酶)可增强对 B. cinerea 的抗病性。同样,Medicago truncatula lha-1 突变体的三萜类皂苷生物合成受到影响,但其抗病性有所增强。有趣的是,不同纯化三萜类皂苷的药理应用补充了 pil 和 hla-1 突变体的抗病表型,并增强了不同植物物种对疾病的敏感性。我们发现,三萜类皂苷作为植物线索,可发出信号,对银环孢菌进行转录重编程,从而改变其生长习性和感染策略,最终大量形成感染垫(IC),这是银环孢菌专门用于植物穿透和生物量破坏的多细胞附生器。我们的研究结果解释了植物三萜类皂苷如何作为疾病易感性因子(S)促进 B. cinerea 的致病性。
{"title":"Plant triterpenoid saponins function as susceptibility factors to promote the pathogenicity of Botrytis cinerea.","authors":"Francisco J Escaray, Amelia Felipo-Benavent, Cristian J Antonelli, Begoña Balaguer, Maria Pilar Lopez-Gresa, Pablo Vera","doi":"10.1016/j.molp.2024.05.008","DOIUrl":"10.1016/j.molp.2024.05.008","url":null,"abstract":"<p><p>The gray mold fungus Botrytis cinerea is a necrotrophic pathogen that causes diseases in hundreds of plant species, including high-value crops. Its polyxenous nature and pathogenic success are due to its ability to perceive host signals in its favor. In this study, we found that laticifer cells of Euphorbia lathyris are a source of susceptibility factors required by B. cinerea to cause disease. Consequently, poor-in-latex (pil) mutants, which lack laticifer cells, show full resistance to this pathogen, whereas lot-of-latex mutants, which produce more laticifer cells, are hypersusceptible. These S factors are triterpenoid saponins, which are widely distributed natural products of vast structural diversity. The downregulation of laticifer-specific oxydosqualene cyclase genes, which encode the first committed step enzymes for triterpene and, therefore, saponin biosynthesis, conferred disease resistance to B. cinerea. Likewise, the Medicago truncatula lha-1 mutant, compromised in triterpenoid saponin biosynthesis, showed enhanced resistance. Interestingly, the application of different purified triterpenoid saponins pharmacologically complemented the disease-resistant phenotype of pil and hla-1 mutants and enhanced disease susceptibility in different plant species. We found that triterpenoid saponins function as plant cues that signal transcriptional reprogramming in B. cinerea, leading to a change in its growth habit and infection strategy, culminating in the abundant formation of infection cushions, the multicellular appressoria apparatus dedicated to plant penetration and biomass destruction in B. cinerea. Taken together, these results provide an explanation for how plant triterpenoid saponins function as disease susceptibility factors to promote B. cinerea pathogenicity.</p>","PeriodicalId":19012,"journal":{"name":"Molecular Plant","volume":" ","pages":"1073-1089"},"PeriodicalIF":17.1,"publicationDate":"2024-07-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141162267","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}