Gabriel Gómez-Ocampo, Carlos D Crocco, Jimena Cascales, Jana Oklestkova, Danuše Tarkowská, Miroslav Strnad, Santiago Mora-Garcia, José L Pruneda-Paz, Miguel A Blazquez, Javier F Botto
B-Box-containing zinc finger transcription factors (BBX) are involved in light-mediated growth, affecting processes such as hypocotyl elongation in Arabidopsis thaliana. However, the molecular and hormonal framework that regulates plant growth through BBX proteins is incomplete. Here, we demonstrate that BBX21 inhibits the hypocotyl elongation through the brassinosteroid (BR) pathway. BBX21 reduces the sensitivity to 24-epiBL, a synthetic active BR, principally at very low concentrations in simulated shade. The biosynthesis profile of BRs showed that two active BR-brassinolide and 28-homobrassinolide-and 8 of 11 intermediates can be repressed by BBX21 under white light (WL) or simulated shade. Furthermore, BBX21 represses the expression of CYTOCHROME P450 90B1 (DWF4/CYP90B1), BRASSINOSTEROID-6-OXIDASE 1 (BR6OX1, CYP85A1) and BR6OX2 (CYP85A2) genes involved in the BR biosynthesis in WL while specifically promoting DWF4 and PHYB ACTIVATION TAGGED SUPPRESSOR 1 (CYP2B1/BAS1) expression in WL supplemented with far-red (WL + FR), a treatment that simulates shade. In addition, BBX21 represses BR signaling genes, such as PACLOBUTRAZOL RESISTANCE1 (PRE1), PRE3 and ARABIDOPSIS MYB-LIKE 2 (MYBL2), and auxin-related and expansin genes, such as INDOLE-3-ACETIC ACID INDUCIBLE 1 (IAA1), IAA4 and EXPANSIN 11 in short-term shade. By a genetic approach, we found that BBX21 acts genetically upstream of BRASSINAZOLE-RESISTANT 1 (BZR1) for the promotion of DWF4 and BAS1 gene expression in shade. We propose that BBX21 integrates the BR homeostasis and shade-light signaling, allowing the fine-tuning of hypocotyl elongation in Arabidopsis.
{"title":"BBX21 Integrates Brassinosteroid Biosynthesis and Signaling in the Inhibition of Hypocotyl Growth under Shade.","authors":"Gabriel Gómez-Ocampo, Carlos D Crocco, Jimena Cascales, Jana Oklestkova, Danuše Tarkowská, Miroslav Strnad, Santiago Mora-Garcia, José L Pruneda-Paz, Miguel A Blazquez, Javier F Botto","doi":"10.1093/pcp/pcad126","DOIUrl":"10.1093/pcp/pcad126","url":null,"abstract":"<p><p>B-Box-containing zinc finger transcription factors (BBX) are involved in light-mediated growth, affecting processes such as hypocotyl elongation in Arabidopsis thaliana. However, the molecular and hormonal framework that regulates plant growth through BBX proteins is incomplete. Here, we demonstrate that BBX21 inhibits the hypocotyl elongation through the brassinosteroid (BR) pathway. BBX21 reduces the sensitivity to 24-epiBL, a synthetic active BR, principally at very low concentrations in simulated shade. The biosynthesis profile of BRs showed that two active BR-brassinolide and 28-homobrassinolide-and 8 of 11 intermediates can be repressed by BBX21 under white light (WL) or simulated shade. Furthermore, BBX21 represses the expression of CYTOCHROME P450 90B1 (DWF4/CYP90B1), BRASSINOSTEROID-6-OXIDASE 1 (BR6OX1, CYP85A1) and BR6OX2 (CYP85A2) genes involved in the BR biosynthesis in WL while specifically promoting DWF4 and PHYB ACTIVATION TAGGED SUPPRESSOR 1 (CYP2B1/BAS1) expression in WL supplemented with far-red (WL + FR), a treatment that simulates shade. In addition, BBX21 represses BR signaling genes, such as PACLOBUTRAZOL RESISTANCE1 (PRE1), PRE3 and ARABIDOPSIS MYB-LIKE 2 (MYBL2), and auxin-related and expansin genes, such as INDOLE-3-ACETIC ACID INDUCIBLE 1 (IAA1), IAA4 and EXPANSIN 11 in short-term shade. By a genetic approach, we found that BBX21 acts genetically upstream of BRASSINAZOLE-RESISTANT 1 (BZR1) for the promotion of DWF4 and BAS1 gene expression in shade. We propose that BBX21 integrates the BR homeostasis and shade-light signaling, allowing the fine-tuning of hypocotyl elongation in Arabidopsis.</p>","PeriodicalId":20575,"journal":{"name":"Plant and Cell Physiology","volume":" ","pages":"1627-1639"},"PeriodicalIF":3.9,"publicationDate":"2024-11-13","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"41238083","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Brassinosteroids (BRs) are a group of polyhydroxylated phytosterols that play essential roles in regulating plant growth and development as well as stress adaptation. It is worth noting that BRs do not function alone, but rather they crosstalk with other endogenous signaling molecules, including the phytohormones auxin, cytokinins, gibberellins, abscisic acid, ethylene, jasmonates, salicylic acid and strigolactones, forming elaborate signaling networks to modulate plant growth and development. BRs interact with other phytohormones mainly by regulating each others' homeostasis, transport or signaling pathway at the transcriptional and posttranslational levels. In this review, we focus our attention on current research progress in BR signal transduction and the crosstalk between BRs and other phytohormones.
{"title":"Crosstalk between Brassinosteroids and Other Phytohormones during Plant Development and Stress Adaptation.","authors":"Feimei Guo, Minghui Lv, Jingjie Zhang, Jia Li","doi":"10.1093/pcp/pcae047","DOIUrl":"10.1093/pcp/pcae047","url":null,"abstract":"<p><p>Brassinosteroids (BRs) are a group of polyhydroxylated phytosterols that play essential roles in regulating plant growth and development as well as stress adaptation. It is worth noting that BRs do not function alone, but rather they crosstalk with other endogenous signaling molecules, including the phytohormones auxin, cytokinins, gibberellins, abscisic acid, ethylene, jasmonates, salicylic acid and strigolactones, forming elaborate signaling networks to modulate plant growth and development. BRs interact with other phytohormones mainly by regulating each others' homeostasis, transport or signaling pathway at the transcriptional and posttranslational levels. In this review, we focus our attention on current research progress in BR signal transduction and the crosstalk between BRs and other phytohormones.</p>","PeriodicalId":20575,"journal":{"name":"Plant and Cell Physiology","volume":" ","pages":"1530-1543"},"PeriodicalIF":3.9,"publicationDate":"2024-11-13","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"140899336","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
The polyhydroxylated steroid phytohormone brassinosteroid (BR) controls many aspects of plant growth, development and responses to environmental changes. Plasma membrane (PM) H+-ATPase, the well-known PM proton pump, is a central regulator in plant physiology, which mediates not only plant growth and development, but also adaptation to stresses. Recent studies highlight that PM H+-ATPase is at least partly regulated via the BR signaling. Firstly, the BR cell surface receptor BRASSINOSTEROID-INSENSITIVE 1 (BRI1) and multiple key components of BR signaling directly or indirectly influence PM H+-ATPase activity. Secondly, the SMALL AUXIN UP RNA (SAUR) gene family physically interacts with BRI1 to enhance organ development of Arabidopsis by activating PM H+-ATPase. Thirdly, RNA-sequencing (RNA-seq) assays showed that the expression of some SAUR genes is upregulated under the light or sucrose conditions, which is related to the phosphorylation state of the penultimate residue of PM H+-ATPase in a time-course manner. In this review, we describe the structural and functional features of PM H+-ATPase and summarize recent progress towards understanding the regulatory mechanism of PM H+-ATPase by BRs, and briefly introduce how PM H+-ATPase activity is modulated by its own biterminal regions and the post-translational modifications.
{"title":"Recent Advances in Understanding the Regulatory Mechanism of Plasma Membrane H+-ATPase through the Brassinosteroid Signaling Pathway.","authors":"Zhaoheng Lin, Pan Zhu, Liyang Gao, Xuanyi Chen, Meijing Li, Yuhe Wang, Junxian He, Ying Miao, Rui Miao","doi":"10.1093/pcp/pcae014","DOIUrl":"10.1093/pcp/pcae014","url":null,"abstract":"<p><p>The polyhydroxylated steroid phytohormone brassinosteroid (BR) controls many aspects of plant growth, development and responses to environmental changes. Plasma membrane (PM) H+-ATPase, the well-known PM proton pump, is a central regulator in plant physiology, which mediates not only plant growth and development, but also adaptation to stresses. Recent studies highlight that PM H+-ATPase is at least partly regulated via the BR signaling. Firstly, the BR cell surface receptor BRASSINOSTEROID-INSENSITIVE 1 (BRI1) and multiple key components of BR signaling directly or indirectly influence PM H+-ATPase activity. Secondly, the SMALL AUXIN UP RNA (SAUR) gene family physically interacts with BRI1 to enhance organ development of Arabidopsis by activating PM H+-ATPase. Thirdly, RNA-sequencing (RNA-seq) assays showed that the expression of some SAUR genes is upregulated under the light or sucrose conditions, which is related to the phosphorylation state of the penultimate residue of PM H+-ATPase in a time-course manner. In this review, we describe the structural and functional features of PM H+-ATPase and summarize recent progress towards understanding the regulatory mechanism of PM H+-ATPase by BRs, and briefly introduce how PM H+-ATPase activity is modulated by its own biterminal regions and the post-translational modifications.</p>","PeriodicalId":20575,"journal":{"name":"Plant and Cell Physiology","volume":" ","pages":"1515-1529"},"PeriodicalIF":3.9,"publicationDate":"2024-11-13","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"139900282","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Drought stress is a major threat leading to global plant and crop losses in the context of the climate change crisis. Brassinosteroids (BRs) are plant steroid hormones, and the BR signaling mechanism in plant development has been well elucidated. Nevertheless, the specific mechanisms of BR signaling in drought stress are still unclear. Here, we identify a novel Arabidopsis gene, BRZ INSENSITIVE LONG HYPOCOTYL 9 (BIL9), which promotes plant growth via BR signaling. Overexpression of BIL9 enhances drought and mannitol stress resistance and increases the expression of drought-responsive genes. BIL9 protein is induced by dehydration and interacts with the HD-Zip IV transcription factor HOMEODOMAIN GLABROUS 11 (HDG11), which is known to promote plant resistance to drought stress, in vitro and in vivo. BIL9 enhanced the transcriptional activity of HDG11 for drought-stress-resistant genes. BIL9 is a novel BR signaling factor that enhances both plant growth and plant drought resistance.
在气候变化危机的背景下,干旱胁迫是导致全球植物和作物损失的主要威胁。芸苔素甾醇(BRs)是植物甾体激素,BR在植物生长发育中的信号转导机制已被阐明。然而,干旱胁迫下芸薹素类固醇信号转导的具体机制仍不清楚。在这里,我们发现了一个新的拟南芥基因--BRZ INSENSITIVE LONG HYPOCOTYL 9(BIL9),它能通过BR信号促进植物生长。过表达 BIL9 可增强干旱和甘露醇胁迫抗性,并增加干旱响应基因的表达。BIL9 蛋白由脱水诱导,并与 HD-Zip IV 转录因子 HOMEODOMAIN GLABROUS 11(HDG11)相互作用,HDG11 在体外和体内都能促进植物对干旱胁迫的抗性。BIL9 增强了 HDG11 对抗旱基因的转录活性。BIL9是一种新型的BR信号转导因子,它既能促进植物生长,又能增强植物的抗旱性。
{"title":"BIL9 Promotes Both Plant Growth via BR Signaling and Drought Stress Resistance by Binding with the Transcription Factor HDG11.","authors":"Surina Surina, Ayumi Yamagami, Tomoko Miyaji, Zhana Chagan, KwiMi Chung, Nobutaka Mitsuda, Kaisei Nishida, Ryo Tachibana, Zhangliang Zhu, Takuya Miyakawa, Kazuo Shinozaki, Masaaki Sakuta, Tadao Asami, Takeshi Nakano","doi":"10.1093/pcp/pcae009","DOIUrl":"10.1093/pcp/pcae009","url":null,"abstract":"<p><p>Drought stress is a major threat leading to global plant and crop losses in the context of the climate change crisis. Brassinosteroids (BRs) are plant steroid hormones, and the BR signaling mechanism in plant development has been well elucidated. Nevertheless, the specific mechanisms of BR signaling in drought stress are still unclear. Here, we identify a novel Arabidopsis gene, BRZ INSENSITIVE LONG HYPOCOTYL 9 (BIL9), which promotes plant growth via BR signaling. Overexpression of BIL9 enhances drought and mannitol stress resistance and increases the expression of drought-responsive genes. BIL9 protein is induced by dehydration and interacts with the HD-Zip IV transcription factor HOMEODOMAIN GLABROUS 11 (HDG11), which is known to promote plant resistance to drought stress, in vitro and in vivo. BIL9 enhanced the transcriptional activity of HDG11 for drought-stress-resistant genes. BIL9 is a novel BR signaling factor that enhances both plant growth and plant drought resistance.</p>","PeriodicalId":20575,"journal":{"name":"Plant and Cell Physiology","volume":" ","pages":"1640-1654"},"PeriodicalIF":3.9,"publicationDate":"2024-11-13","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"139502765","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
5β-Cardenolides are pharmaceutically important metabolites from the specialized metabolism of Digitalis lanata. They were used over decades to treat cardiac insufficiency and supraventricular tachycardia. Since the 1960s, plant scientists have known that progesterone is an essential precursor of cardenolide formation. Therefore, biosynthesis of plant progesterone was mainly analyzed in species of the cardenolide-containing genus Digitalis during the following decades. Today, Digitalis enzymes catalyzing the main steps of progesterone biosynthesis are known. Most of them are found in a broad range of organisms. This review will summarize the findings of 60 years of research on plant progesterone metabolism with particular focus on the recent results in Digitalis lanata and other plants.
{"title":"Progesterone Metabolism in Digitalis and Other Plants-60 Years of Research and Recent Results.","authors":"Jan Klein","doi":"10.1093/pcp/pcae006","DOIUrl":"10.1093/pcp/pcae006","url":null,"abstract":"<p><p>5β-Cardenolides are pharmaceutically important metabolites from the specialized metabolism of Digitalis lanata. They were used over decades to treat cardiac insufficiency and supraventricular tachycardia. Since the 1960s, plant scientists have known that progesterone is an essential precursor of cardenolide formation. Therefore, biosynthesis of plant progesterone was mainly analyzed in species of the cardenolide-containing genus Digitalis during the following decades. Today, Digitalis enzymes catalyzing the main steps of progesterone biosynthesis are known. Most of them are found in a broad range of organisms. This review will summarize the findings of 60 years of research on plant progesterone metabolism with particular focus on the recent results in Digitalis lanata and other plants.</p>","PeriodicalId":20575,"journal":{"name":"Plant and Cell Physiology","volume":" ","pages":"1500-1514"},"PeriodicalIF":3.9,"publicationDate":"2024-11-13","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"139472104","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
High-temperature stress (HTS) affects the growth and production of vegetable crops, including eggplant (Solanum melongena L.). Jasmonic acid (JA) plays key roles in regulating resistance to biotic and abiotic stresses in plants. Nonetheless, reports on the role of JA in heat tolerance in eggplant are rare. Herein, the effects of JA on heat tolerance in eggplant and the functions of the JA biosynthetic genes SmLOX4 and SmLOX5 were analyzed. The results showed that the JA content increased under high-temperature treatment (HTT) and exogenous methyl jasmonate (MeJA) treatment reduced the damage caused by HTT to eggplant. The expression of SmLOX4 and SmLOX5 was induced by HTT and significantly positively correlated with JA biosynthesis. SmLOX4 and SmLOX5 were localized in chloroplasts. The silencing of SmLOX4 and SmLOX5 by virus-induced gene silencing suppressed the heat tolerance of eggplant, whereas the overexpression of SmLOX4 and SmLOX5 enhanced the heat tolerance of Arabidopsis thaliana. JA content and the expression of JA signaling-related genes decreased in the SmLOX4- and SmLOX5-silenced plants but increased in the OE-SmLOX4 and OE-SmLOX5 transgenic plants. These results revealed that SmLOX4 and SmLOX5 improved eggplant heat tolerance by mediating JA biosynthesis and JA signaling pathways.
高温胁迫(HTS)会影响包括茄子(Solanum melongena L.)在内的蔬菜作物的生长和产量。茉莉酸(JA)在调节植物对生物和非生物胁迫的抗性方面发挥着关键作用。然而,有关 JA 在茄子耐热性中的作用的报道却很少见。本文分析了 JA 对茄子耐热性的影响以及 JA 生物合成基因 SmLOX4 和 SmLOX5 的功能。结果表明,在高温处理(HTT)下,JA含量增加,外源茉莉酸甲酯(MeJA)处理减轻了高温处理对茄子的伤害。HTT诱导了SmLOX4和SmLOX5的表达,并与JA的生物合成显著正相关。SmLOX4 和 SmLOX5 定位于叶绿体中。通过病毒诱导基因沉默(VIGS)沉默SmLOX4和SmLOX5抑制了茄子植株的耐热性,而过表达SmLOX4和SmLOX5增强了拟南芥植株的耐热性。SmLOX4和SmLOX5沉默植株的JA含量和JA信号相关基因的表达量减少,而OE-SmLOX4和OE-SmLOX5转基因植株的JA含量和JA信号相关基因的表达量增加。这些结果表明,SmLOX4 和 SmLOX5 通过介导 JA 生物合成和 JA 信号途径提高了茄子的耐热性。
{"title":"The Jasmonic Acid Biosynthetic Genes SmLOX4 and SmLOX5 Are Involved in Heat Tolerance in Eggplant.","authors":"Renjian Liu, Bingbing Shu, Yuyuan Wang, Jiazhu Feng, Bingwei Yu, Yuwei Gan, Yonggui Liang, Zhengkun Qiu, Shuangshuang Yan, Bihao Cao","doi":"10.1093/pcp/pcae088","DOIUrl":"10.1093/pcp/pcae088","url":null,"abstract":"<p><p>High-temperature stress (HTS) affects the growth and production of vegetable crops, including eggplant (Solanum melongena L.). Jasmonic acid (JA) plays key roles in regulating resistance to biotic and abiotic stresses in plants. Nonetheless, reports on the role of JA in heat tolerance in eggplant are rare. Herein, the effects of JA on heat tolerance in eggplant and the functions of the JA biosynthetic genes SmLOX4 and SmLOX5 were analyzed. The results showed that the JA content increased under high-temperature treatment (HTT) and exogenous methyl jasmonate (MeJA) treatment reduced the damage caused by HTT to eggplant. The expression of SmLOX4 and SmLOX5 was induced by HTT and significantly positively correlated with JA biosynthesis. SmLOX4 and SmLOX5 were localized in chloroplasts. The silencing of SmLOX4 and SmLOX5 by virus-induced gene silencing suppressed the heat tolerance of eggplant, whereas the overexpression of SmLOX4 and SmLOX5 enhanced the heat tolerance of Arabidopsis thaliana. JA content and the expression of JA signaling-related genes decreased in the SmLOX4- and SmLOX5-silenced plants but increased in the OE-SmLOX4 and OE-SmLOX5 transgenic plants. These results revealed that SmLOX4 and SmLOX5 improved eggplant heat tolerance by mediating JA biosynthesis and JA signaling pathways.</p>","PeriodicalId":20575,"journal":{"name":"Plant and Cell Physiology","volume":" ","pages":"1705-1716"},"PeriodicalIF":3.9,"publicationDate":"2024-11-13","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11558548/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141907574","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Taehoon Kim, Javier C Alvarez, Divya Rana, Jesus Preciado, Tie Liu, Kevin Begcy
NAC [NO APICAL MERISTEM (NAM), ARABIDOPSIS TRANSCRIPTION ACTIVATOR FACTOR 1/2 (ATAF1/2), and CUP-SHAPED COTYLEDON (CUC2)] transcription factors are key regulators of plant growth, development, and stress responses but were also crucial players during land plant adaptation and crop domestication. Using representative members of green algae, bryophytes, lycophytes, gymnosperms, and angiosperms, we expanded the evolutionary history of NAC transcription factors to unveil the relationships among members of this gene family. We found a massive increase in the number of NAC transcription factors from green algae to lycophytes and an even larger increase in flowering plants. Many of the NAC clades arose later during evolution since we found eudicot- and monocot-specific clades. Cis-elements analysis in NAC promoters showed the presence of abiotic and biotic stress as well as hormonal response elements, which indicate the ancestral function of NAC transcription factor genes in response to environmental stimuli and in plant development. At the transcriptional level, the expression of NAC transcription factors was low or absent in male reproduction, particularly mature pollen, across the plant kingdom. We also identified NAC genes with conserved expression patterns in response to heat stress in Marchantia polymorpha and Oryza sativa. Our study provides further evidence that transcriptional mechanisms associated with stress responses and development emerged early during plant land adaptation and are still conserved in flowering plants and domesticated crops.
{"title":"Evolution of NAC transcription factors from early land plants to domesticated crops.","authors":"Taehoon Kim, Javier C Alvarez, Divya Rana, Jesus Preciado, Tie Liu, Kevin Begcy","doi":"10.1093/pcp/pcae133","DOIUrl":"https://doi.org/10.1093/pcp/pcae133","url":null,"abstract":"<p><p>NAC [NO APICAL MERISTEM (NAM), ARABIDOPSIS TRANSCRIPTION ACTIVATOR FACTOR 1/2 (ATAF1/2), and CUP-SHAPED COTYLEDON (CUC2)] transcription factors are key regulators of plant growth, development, and stress responses but were also crucial players during land plant adaptation and crop domestication. Using representative members of green algae, bryophytes, lycophytes, gymnosperms, and angiosperms, we expanded the evolutionary history of NAC transcription factors to unveil the relationships among members of this gene family. We found a massive increase in the number of NAC transcription factors from green algae to lycophytes and an even larger increase in flowering plants. Many of the NAC clades arose later during evolution since we found eudicot- and monocot-specific clades. Cis-elements analysis in NAC promoters showed the presence of abiotic and biotic stress as well as hormonal response elements, which indicate the ancestral function of NAC transcription factor genes in response to environmental stimuli and in plant development. At the transcriptional level, the expression of NAC transcription factors was low or absent in male reproduction, particularly mature pollen, across the plant kingdom. We also identified NAC genes with conserved expression patterns in response to heat stress in Marchantia polymorpha and Oryza sativa. Our study provides further evidence that transcriptional mechanisms associated with stress responses and development emerged early during plant land adaptation and are still conserved in flowering plants and domesticated crops.</p>","PeriodicalId":20575,"journal":{"name":"Plant and Cell Physiology","volume":" ","pages":""},"PeriodicalIF":3.9,"publicationDate":"2024-11-12","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142886157","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Ryo A Suda, Shosei Kubota, Vinod Kumar, Vincent Castric, Ute Krämer, Shin-Ichi Morinaga, Takashi Tsuchimatsu
Climate oscillations in the Quaternary forced species to major latitudinal or altitudinal range shifts. It has been suggested that adaptation concomitant with range shifts plays key roles in species responses during climate oscillations, but the role of selection for local adaptation to climatic changes remains largely unexplored. Here, we investigated population structure, demographic history and signatures of climate-driven selection based on genome-wide polymorphism data of 141 Japanese Arabidopsis halleri individuals, with European ones as outgroups. Coalescent-based analyses suggested a genetic differentiation between Japanese subpopulations since the Last Glacial Period (LGP), which would have contributed to shaping the current pattern of population structure. Population demographic analysis revealed the population size fluctuations in the LGP, which were particularly prominent since the subpopulations started to diverge (∼50, 000 years ago). The ecological niche modeling predicted the geographic or distribution range shifts from southern coastal regions to northern coastal and mountainous areas, possibly in association with the population size fluctuations. Through genome-wide association analyses of bioclimatic variables and selection scans, we investigated whether climate-associated loci are enriched in the extreme tails of selection scans, and demonstrated the prevailing signatures of selection, particularly toward a warmer climate in southern subpopulations and a drier environment in northern subpopulations, which may have taken place during or after the LGP. Our study highlights the importance of integrating climate associations, selection scans and population demographic analyses for identifying genomic signatures of population-specific adaptation, which would also help us predict the evolutionary responses to future climate changes.
{"title":"Population Genomics Reveals Demographic History and Climate Adaptation in Japanese Arabidopsis halleri.","authors":"Ryo A Suda, Shosei Kubota, Vinod Kumar, Vincent Castric, Ute Krämer, Shin-Ichi Morinaga, Takashi Tsuchimatsu","doi":"10.1093/pcp/pcae113","DOIUrl":"https://doi.org/10.1093/pcp/pcae113","url":null,"abstract":"<p><p>Climate oscillations in the Quaternary forced species to major latitudinal or altitudinal range shifts. It has been suggested that adaptation concomitant with range shifts plays key roles in species responses during climate oscillations, but the role of selection for local adaptation to climatic changes remains largely unexplored. Here, we investigated population structure, demographic history and signatures of climate-driven selection based on genome-wide polymorphism data of 141 Japanese Arabidopsis halleri individuals, with European ones as outgroups. Coalescent-based analyses suggested a genetic differentiation between Japanese subpopulations since the Last Glacial Period (LGP), which would have contributed to shaping the current pattern of population structure. Population demographic analysis revealed the population size fluctuations in the LGP, which were particularly prominent since the subpopulations started to diverge (∼50, 000 years ago). The ecological niche modeling predicted the geographic or distribution range shifts from southern coastal regions to northern coastal and mountainous areas, possibly in association with the population size fluctuations. Through genome-wide association analyses of bioclimatic variables and selection scans, we investigated whether climate-associated loci are enriched in the extreme tails of selection scans, and demonstrated the prevailing signatures of selection, particularly toward a warmer climate in southern subpopulations and a drier environment in northern subpopulations, which may have taken place during or after the LGP. Our study highlights the importance of integrating climate associations, selection scans and population demographic analyses for identifying genomic signatures of population-specific adaptation, which would also help us predict the evolutionary responses to future climate changes.</p>","PeriodicalId":20575,"journal":{"name":"Plant and Cell Physiology","volume":" ","pages":""},"PeriodicalIF":3.9,"publicationDate":"2024-11-06","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142583552","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Understanding plant responses to developmental and environmental cues is crucial for studying morphological divergence and local adaptation. Gene expression changes, governed by cis-regulatory modules (CRMs) including enhancers, are a major source of plant phenotypic variation. However, while genome-wide approaches have revealed thousands of putative enhancers in mammals, far fewer have been identified and functionally characterized in plants. This review provides an overview of how enhancers function to control gene regulation, methods to predict DNA sequences that may have enhancer activity, methods utilized to functionally validate enhancers, and the current knowledge of enhancers in plants, including how they impact plant development, response to environment, and evolutionary adaptation.
了解植物对发育和环境线索的反应对于研究形态差异和局部适应至关重要。由包括增强子在内的顺式调控模块(CRM)控制的基因表达变化是植物表型变异的主要来源。然而,尽管全基因组方法在哺乳动物中发现了数千个假定的增强子,但在植物中发现的增强子数量和功能特征却少得多。本综述概述了增强子如何发挥控制基因调控的功能、预测可能具有增强子活性的 DNA 序列的方法、对增强子进行功能验证的方法,以及目前对植物中增强子的了解,包括它们如何影响植物的发育、对环境的响应以及进化适应。
{"title":"Enhancers in Plant Development, Adaptation, and Evolution.","authors":"Bliss M Beernink, John P Vogel, Li Lei","doi":"10.1093/pcp/pcae121","DOIUrl":"https://doi.org/10.1093/pcp/pcae121","url":null,"abstract":"<p><p>Understanding plant responses to developmental and environmental cues is crucial for studying morphological divergence and local adaptation. Gene expression changes, governed by cis-regulatory modules (CRMs) including enhancers, are a major source of plant phenotypic variation. However, while genome-wide approaches have revealed thousands of putative enhancers in mammals, far fewer have been identified and functionally characterized in plants. This review provides an overview of how enhancers function to control gene regulation, methods to predict DNA sequences that may have enhancer activity, methods utilized to functionally validate enhancers, and the current knowledge of enhancers in plants, including how they impact plant development, response to environment, and evolutionary adaptation.</p>","PeriodicalId":20575,"journal":{"name":"Plant and Cell Physiology","volume":" ","pages":""},"PeriodicalIF":3.9,"publicationDate":"2024-10-16","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142473128","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Extreme environments and plants thriving in them, known as extremophytes, offer promising platforms for studying the diverse adaptive mechanisms that have evolved in plants. However, research on adaptation to extreme environments is still limited to those environments where model species or their relative can survive. Fumarole fields, an extreme environment often overlooked, are characterized by multi-hazardous abiotic stressors, including atmospheric contamination (high concentration of H2S, SO2, and CO2), high soil temperature (~60℃), and strong soil acidification (pH=2-3). These conditions make fumarole fields a rich source for studying stress tolerance mechanisms in plants. In this review, we highlight the recent ecological, physiological, and genomic advances involved in fumarole field adaptation, and discuss the forward avenues. The studies outlined in this paper demonstrate that the extreme levels of abiotic stressors found in fumarole fields make them unparalleled field laboratories for studying the unknown stress tolerance mechanisms, warranting further genomic assessments. Some studies succeeded in identifying genes associated with fumarole field adaptation and shedding light on evolutionary implications; however, they have also encountered challenges such as limited genome resources and high genetic differentiation from related species and/or neighboring populations. To overcome such difficulties, we propose integrating ecophysiological and genomic approaches, drawing from the recent studies in other extreme environments. We expect that further studies in the fumarole fields will contribute to broadening our general knowledge of the limits of life.
{"title":"Recent advances in adaptation genomics in fumarole fields, an overlooked extreme environment.","authors":"Koki Nagasawa, Hiroaki Setoguchi, Shota Sakaguchi","doi":"10.1093/pcp/pcae122","DOIUrl":"https://doi.org/10.1093/pcp/pcae122","url":null,"abstract":"<p><p>Extreme environments and plants thriving in them, known as extremophytes, offer promising platforms for studying the diverse adaptive mechanisms that have evolved in plants. However, research on adaptation to extreme environments is still limited to those environments where model species or their relative can survive. Fumarole fields, an extreme environment often overlooked, are characterized by multi-hazardous abiotic stressors, including atmospheric contamination (high concentration of H2S, SO2, and CO2), high soil temperature (~60℃), and strong soil acidification (pH=2-3). These conditions make fumarole fields a rich source for studying stress tolerance mechanisms in plants. In this review, we highlight the recent ecological, physiological, and genomic advances involved in fumarole field adaptation, and discuss the forward avenues. The studies outlined in this paper demonstrate that the extreme levels of abiotic stressors found in fumarole fields make them unparalleled field laboratories for studying the unknown stress tolerance mechanisms, warranting further genomic assessments. Some studies succeeded in identifying genes associated with fumarole field adaptation and shedding light on evolutionary implications; however, they have also encountered challenges such as limited genome resources and high genetic differentiation from related species and/or neighboring populations. To overcome such difficulties, we propose integrating ecophysiological and genomic approaches, drawing from the recent studies in other extreme environments. We expect that further studies in the fumarole fields will contribute to broadening our general knowledge of the limits of life.</p>","PeriodicalId":20575,"journal":{"name":"Plant and Cell Physiology","volume":" ","pages":""},"PeriodicalIF":3.9,"publicationDate":"2024-10-16","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142473130","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}