Plant CommunicationsPub Date : 2024-06-10Epub Date: 2024-02-19DOI: 10.1016/j.xplc.2024.100848
Tom Rankenberg, Hans van Veen, Mastoureh Sedaghatmehr, Che-Yang Liao, Muthanna Biddanda Devaiah, Evelien A Stouten, Salma Balazadeh, Rashmi Sasidharan
{"title":"Differential leaf flooding resilience in Arabidopsis thaliana is controlled by ethylene signaling-activated and age-dependent phosphorylation of ORESARA1.","authors":"Tom Rankenberg, Hans van Veen, Mastoureh Sedaghatmehr, Che-Yang Liao, Muthanna Biddanda Devaiah, Evelien A Stouten, Salma Balazadeh, Rashmi Sasidharan","doi":"10.1016/j.xplc.2024.100848","DOIUrl":"10.1016/j.xplc.2024.100848","url":null,"abstract":"<p><p>The phytohormone ethylene is a major regulator of plant adaptive responses to flooding. In flooded plant tissues, ethylene quickly increases to high concentrations owing to its low solubility and diffusion rates in water. Ethylene accumulation in submerged plant tissues makes it a reliable cue for triggering flood acclimation responses, including metabolic adjustments to cope with flood-induced hypoxia. However, persistent ethylene accumulation also accelerates leaf senescence. Stress-induced senescence hampers photosynthetic capacity and stress recovery. In submerged Arabidopsis, senescence follows a strict age-dependent pattern starting with the older leaves. Although mechanisms underlying ethylene-mediated senescence have been uncovered, it is unclear how submerged plants avoid indiscriminate breakdown of leaves despite high systemic ethylene accumulation. We demonstrate that although submergence triggers leaf-age-independent activation of ethylene signaling via EIN3 in Arabidopsis, senescence is initiated only in old leaves. EIN3 stabilization also leads to overall transcript and protein accumulation of the senescence-promoting transcription factor ORESARA1 (ORE1) in both old and young leaves during submergence. However, leaf-age-dependent senescence can be explained by ORE1 protein activation via phosphorylation specifically in old leaves, independent of the previously identified age-dependent control of ORE1 via miR164. A systematic analysis of the roles of the major flooding stress cues and signaling pathways shows that only the combination of ethylene and darkness is sufficient to mimic submergence-induced senescence involving ORE1 accumulation and phosphorylation. Hypoxia, most often associated with flooding stress in plants, appears to have no role in these processes. Our results reveal a mechanism by which plants regulate the speed and pattern of senescence during environmental stresses such as flooding. Age-dependent ORE1 activity ensures that older, expendable leaves are dismantled first, thus prolonging the life of younger leaves and meristematic tissues that are vital to whole-plant survival.</p>","PeriodicalId":52373,"journal":{"name":"Plant Communications","volume":null,"pages":null},"PeriodicalIF":9.4,"publicationDate":"2024-06-10","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11211547/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"139914044","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}
Plant CommunicationsPub Date : 2024-06-10Epub Date: 2024-03-08DOI: 10.1016/j.xplc.2024.100846
George Heslop-Harrison, Kazumi Nakabayashi, Ana Espinosa-Ruiz, Francesca Robertson, Robert Baines, Christopher R L Thompson, Katrin Hermann, David Alabadí, Gerhard Leubner-Metzger, Robin S B Williams
{"title":"Functional mechanism study of the allelochemical myrigalone A identifies a group of ultrapotent inhibitors of ethylene biosynthesis in plants.","authors":"George Heslop-Harrison, Kazumi Nakabayashi, Ana Espinosa-Ruiz, Francesca Robertson, Robert Baines, Christopher R L Thompson, Katrin Hermann, David Alabadí, Gerhard Leubner-Metzger, Robin S B Williams","doi":"10.1016/j.xplc.2024.100846","DOIUrl":"10.1016/j.xplc.2024.100846","url":null,"abstract":"<p><p>Allelochemicals represent a class of natural products released by plants as root, leaf, and fruit exudates that interfere with the growth and survival of neighboring plants. Understanding how allelochemicals function to regulate plant responses may provide valuable new approaches to better control plant function. One such allelochemical, Myrigalone A (MyA) produced by Myrica gale, inhibits seed germination and seedling growth through an unknown mechanism. Here, we investigate MyA using the tractable model Dictyostelium discoideum and reveal that its activity depends on the conserved homolog of the plant ethylene synthesis protein 1-aminocyclopropane-1-carboxylic acid oxidase (ACO). Furthermore, in silico modeling predicts the direct binding of MyA to ACO within the catalytic pocket. In D. discoideum, ablation of ACO mimics the MyA-dependent developmental delay, which is partially restored by exogenous ethylene, and MyA reduces ethylene production. In Arabidopsis thaliana, MyA treatment delays seed germination, and this effect is rescued by exogenous ethylene. It also mimics the effect of established ACO inhibitors on root and hypocotyl extension, blocks ethylene-dependent root hair production, and reduces ethylene production. Finally, in silico binding analyses identify a range of highly potent ethylene inhibitors that block ethylene-dependent response and reduce ethylene production in Arabidopsis. Thus, we demonstrate a molecular mechanism by which the allelochemical MyA reduces ethylene biosynthesis and identify a range of ultrapotent inhibitors of ethylene-regulated responses.</p>","PeriodicalId":52373,"journal":{"name":"Plant Communications","volume":null,"pages":null},"PeriodicalIF":9.4,"publicationDate":"2024-06-10","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11211550/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"140068957","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}
Plant CommunicationsPub Date : 2024-06-10Epub Date: 2024-04-15DOI: 10.1016/j.xplc.2024.100920
Carissa Bleker, Živa Ramšak, Andras Bittner, Vid Podpečan, Maja Zagorščak, Bernhard Wurzinger, Špela Baebler, Marko Petek, Maja Križnik, Annelotte van Dieren, Juliane Gruber, Leila Afjehi-Sadat, Wolfram Weckwerth, Anže Županič, Markus Teige, Ute C Vothknecht, Kristina Gruden
{"title":"Stress Knowledge Map: A knowledge graph resource for systems biology analysis of plant stress responses.","authors":"Carissa Bleker, Živa Ramšak, Andras Bittner, Vid Podpečan, Maja Zagorščak, Bernhard Wurzinger, Špela Baebler, Marko Petek, Maja Križnik, Annelotte van Dieren, Juliane Gruber, Leila Afjehi-Sadat, Wolfram Weckwerth, Anže Županič, Markus Teige, Ute C Vothknecht, Kristina Gruden","doi":"10.1016/j.xplc.2024.100920","DOIUrl":"10.1016/j.xplc.2024.100920","url":null,"abstract":"<p><p>Stress Knowledge Map (SKM; https://skm.nib.si) is a publicly available resource containing two complementary knowledge graphs that describe the current knowledge of biochemical, signaling, and regulatory molecular interactions in plants: a highly curated model of plant stress signaling (PSS; 543 reactions) and a large comprehensive knowledge network (488 390 interactions). Both were constructed by domain experts through systematic curation of diverse literature and database resources. SKM provides a single entry point for investigations of plant stress response and related growth trade-offs, as well as interactive explorations of current knowledge. PSS is also formulated as a qualitative and quantitative model for systems biology and thus represents a starting point for a plant digital twin. Here, we describe the features of SKM and show, through two case studies, how it can be used for complex analyses, including systematic hypothesis generation and design of validation experiments, or to gain new insights into experimental observations in plant biology.</p>","PeriodicalId":52373,"journal":{"name":"Plant Communications","volume":null,"pages":null},"PeriodicalIF":9.4,"publicationDate":"2024-06-10","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11211517/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"140871203","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}
{"title":"DeepCBA: A deep learning framework for gene expression prediction in maize based on DNA sequences and chromatin interactions.","authors":"Zhenye Wang, Yong Peng, Jie Li, Jiying Li, Hao Yuan, Shangpo Yang, Xinru Ding, Ao Xie, Jiangling Zhang, Shouzhe Wang, Keqin Li, Jiaqi Shi, Guangjie Xing, Weihan Shi, Jianbing Yan, Jianxiao Liu","doi":"10.1016/j.xplc.2024.100985","DOIUrl":"10.1016/j.xplc.2024.100985","url":null,"abstract":"<p><p>Chromatin interactions create spatial proximity between distal regulatory elements and target genes in the genome, which has an important impact on gene expression, transcriptional regulation, and phenotypic traits. To date, several methods have been developed for predicting gene expression. However, existing methods do not take into consideration the effect of chromatin interactions on target gene expression, thus potentially reducing the accuracy of gene expression prediction and mining of important regulatory elements. In this study, we developed a highly accurate deep learning-based gene expression prediction model (DeepCBA) based on maize chromatin interaction data. Compared with existing models, DeepCBA exhibits higher accuracy in expression classification and expression value prediction. The average Pearson correlation coefficients (PCCs) for predicting gene expression using gene promoter proximal interactions, proximal-distal interactions, and both proximal and distal interactions were 0.818, 0.625, and 0.929, respectively, representing an increase of 0.357, 0.16, and 0.469 over the PCCs obtained with traditional methods that use only gene proximal sequences. Some important motifs were identified through DeepCBA; they were enriched in open chromatin regions and expression quantitative trait loci and showed clear tissue specificity. Importantly, experimental results for the maize flowering-related gene ZmRap2.7 and the tillering-related gene ZmTb1 demonstrated the feasibility of DeepCBA for exploration of regulatory elements that affect gene expression. Moreover, promoter editing and verification of two reported genes (ZmCLE7 and ZmVTE4) demonstrated the utility of DeepCBA for the precise design of gene expression and even for future intelligent breeding. DeepCBA is available at http://www.deepcba.com/ or http://124.220.197.196/.</p>","PeriodicalId":52373,"journal":{"name":"Plant Communications","volume":null,"pages":null},"PeriodicalIF":9.4,"publicationDate":"2024-06-10","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141302058","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}
{"title":"Biosynthetic pathway of prescription cucurbitacin IIa and high-level production of key triterpenoid intermediates in engineered yeast and tobacco.","authors":"Geng Chen, Zhaokuan Guo, Yanyu Shu, Yan Zhao, Lei Qiu, Shaofeng Duan, Yuan Lin, Simei He, Xiaobo Li, Xiaolin Feng, Guisheng Xiang, Bo Nian, Yina Wang, Zhiyuan Li, Chongkang Yang, Yang Shi, Yingchun Lu, Guanze Liu, Shengchao Yang, Guanghui Zhang, Bing Hao","doi":"10.1016/j.xplc.2024.100835","DOIUrl":"10.1016/j.xplc.2024.100835","url":null,"abstract":"<p><p>Cucurbitacin IIa is a triterpenoid isolated exclusively from Hemsleya plants and a non-steroidal anti-inflammatory drug that functions as the main ingredient of prescription Hemslecin capsules and tablets in China. Synthetic biology provides new strategies for production of such valuable cucurbitacins at a large scale; however, the biosynthetic pathway of cucurbitacin IIa has been unknown, and the heterologous production of cucurbitacins in galactose medium has been expensive and low yielding. In this study, we characterized the functions of genes encoding two squalene epoxidases (HcSE1-2), six oxidosqualene cyclases (HcOSC1-6), two CYP450s (HcCYP87D20 and HcCYP81Q59), and an acyltransferase (HcAT1) in cucurbitacin IIa biosynthesis by heterologous expression in Saccharomyces cerevisiae and Nicotiana benthamiana. We achieved high-level production of the key cucurbitacin precursor 11-carbonyl-20β-hydroxy-Cuol from glucose in yeast via modular engineering of the mevalonate pathway and optimization of P450 expression levels. The resulting yields of 46.41 mg/l 11-carbonyl-20β-hydroxy-Cuol and 126.47 mg/l total cucurbitacin triterpenoids in shake flasks are the highest yields yet reported from engineered microbes. Subsequently, production of 11-carbonyl-20β-hydroxy-Cuol by transient gene expression in tobacco resulted in yields of 1.28 mg/g dry weight in leaves. This work reveals the key genes involved in biosynthesis of prescription cucurbitacin IIa and demonstrates that engineered yeast cultivated with glucose can produce high yields of key triterpenoid intermediates. We describe a low-cost and highly efficient platform for rapid screening of candidate genes and high-yield production of pharmacological triterpenoids.</p>","PeriodicalId":52373,"journal":{"name":"Plant Communications","volume":null,"pages":null},"PeriodicalIF":9.4,"publicationDate":"2024-06-10","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11211238/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"139998254","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}
Plant CommunicationsPub Date : 2024-06-10Epub Date: 2024-02-25DOI: 10.1016/j.xplc.2024.100851
Guojin Zhang, Junbo Yang, Caifei Zhang, Bohan Jiao, José L Panero, Jie Cai, Zhi-Rong Zhang, Lian-Ming Gao, Tiangang Gao, Hong Ma
{"title":"Nuclear phylogenomics of Asteraceae with increased sampling provides new insights into convergent morphological and molecular evolution.","authors":"Guojin Zhang, Junbo Yang, Caifei Zhang, Bohan Jiao, José L Panero, Jie Cai, Zhi-Rong Zhang, Lian-Ming Gao, Tiangang Gao, Hong Ma","doi":"10.1016/j.xplc.2024.100851","DOIUrl":"10.1016/j.xplc.2024.100851","url":null,"abstract":"<p><p>Convergent morphological evolution is widespread in flowering plants, and understanding this phenomenon relies on well-resolved phylogenies. Nuclear phylogenetic reconstruction using transcriptome datasets has been successful in various angiosperm groups, but it is limited to taxa with available fresh materials. Asteraceae, which are one of the two largest angiosperm families and are important for both ecosystems and human livelihood, show multiple examples of convergent evolution. Nuclear Asteraceae phylogenies have resolved relationships among most subfamilies and many tribes, but many phylogenetic and evolutionary questions regarding subtribes and genera remain, owing to limited sampling. Here, we increased the sampling for Asteraceae phylogenetic reconstruction using transcriptomes and genome-skimming datasets and produced nuclear phylogenetic trees with 706 species representing two-thirds of recognized subtribes. Ancestral character reconstruction supports multiple convergent evolutionary events in Asteraceae, with gains and losses of bilateral floral symmetry correlated with diversification of some subfamilies and smaller groups, respectively. Presence of the calyx-related pappus may have been especially important for the success of some subtribes and genera. Molecular evolutionary analyses support the likely contribution of duplications of MADS-box and TCP floral regulatory genes to innovations in floral morphology, including capitulum inflorescences and bilaterally symmetric flowers, potentially promoting the diversification of Asteraceae. Subsequent divergences and reductions in CYC2 gene expression are related to the gain and loss of zygomorphic flowers. This phylogenomic work with greater taxon sampling through inclusion of genome-skimming datasets reveals the feasibility of expanded evolutionary analyses using DNA samples for understanding convergent evolution.</p>","PeriodicalId":52373,"journal":{"name":"Plant Communications","volume":null,"pages":null},"PeriodicalIF":9.4,"publicationDate":"2024-06-10","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11211554/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"139974459","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}
Plant CommunicationsPub Date : 2024-06-10Epub Date: 2024-02-19DOI: 10.1016/j.xplc.2024.100847
Yingzi Zhang, Jiajing Jin, Nan Wang, Quan Sun, Di Feng, Shenchao Zhu, Zexin Wang, Shunxin Li, Junli Ye, Lijun Chai, Zongzhou Xie, Xiuxin Deng
{"title":"Cytochrome P450 CitCYP97B modulates carotenoid accumulation diversity by hydroxylating β-cryptoxanthin in Citrus.","authors":"Yingzi Zhang, Jiajing Jin, Nan Wang, Quan Sun, Di Feng, Shenchao Zhu, Zexin Wang, Shunxin Li, Junli Ye, Lijun Chai, Zongzhou Xie, Xiuxin Deng","doi":"10.1016/j.xplc.2024.100847","DOIUrl":"10.1016/j.xplc.2024.100847","url":null,"abstract":"<p><p>Carotenoids in plant foods provide health benefits by functioning as provitamin A. One of the vital provitamin A carotenoids, β-cryptoxanthin, is typically plentiful in citrus fruit. However, little is known about the genetic basis of β-cryptoxanthin accumulation in citrus. Here, we performed a widely targeted metabolomic analysis of 65 major carotenoids and carotenoid derivatives to characterize carotenoid accumulation in Citrus and determine the taxonomic profile of β-cryptoxanthin. We used data from 81 newly sequenced representative accessions and 69 previously sequenced Citrus cultivars to reveal the genetic basis of β-cryptoxanthin accumulation through a genome-wide association study. We identified a causal gene, CitCYP97B, which encodes a cytochrome P450 protein whose substrate and metabolic pathways in land plants were undetermined. We subsequently demonstrated that CitCYP97B functions as a novel monooxygenase that specifically hydroxylates the β-ring of β-cryptoxanthin in a heterologous expression system. In planta experiments provided further evidence that CitCYP97B negatively regulates β-cryptoxanthin content. Using the sequenced Citrus accessions, we found that two critical structural cis-element variations contribute to increased expression of CitCYP97B, thereby altering β-cryptoxanthin accumulation in fruit. Hybridization/introgression appear to have contributed to the prevalence of two cis-element variations in different Citrus types during citrus evolution. Overall, these findings extend our understanding of the regulation and diversity of carotenoid metabolism in fruit crops and provide a genetic target for production of β-cryptoxanthin-biofortified products.</p>","PeriodicalId":52373,"journal":{"name":"Plant Communications","volume":null,"pages":null},"PeriodicalIF":9.4,"publicationDate":"2024-06-10","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11211522/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"139914043","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}
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