Nourishing the embryo with endosperm and enclosing both embryo and endosperm in the seed coat are two important evolutionary innovations. Seed coat is conventionally viewed as a protective layer that functions after the seed has matured. Here, we challenge this notion by showing that a subregion of the seed coat, termed the chalazal seed coat (CZSC), is geared to gate seed nutrition loading in developing seeds. The CZSC develops the coordinative system comprising the apoplastic isolation, mediated by the restricted suberization, and the active transport, mediated by the specific expression of a variety of transporters, at as early as the globular embryo stage in both Arabidopsis and soybean seeds. This coordinated system in the CZSC disrupts the vascular continuum to the maternal tissues and forces the nutrient transport into selective and active absorption. We further reveal that the precision of the spatiotemporal suberin deposition and transporter expression is controlled by the regulatory hierarchy of SHR-MYBs cascades. Our results provide a mechanistic insight into the assimilate accumulation in dicot seeds.
{"title":"SHORT-ROOT specifically functions in the chalazal region to modulate assimilate partitioning into seeds.","authors":"Meng Li, Qianfang Li, Shuang Li, Xufang Niu, Huimin Xu, Pengxue Li, Xinxin Bian, Zhichang Chen, Qian Liu, Hongxiang Zhang, Yunqi Liu, Shuang Wu","doi":"10.1111/tpj.17096","DOIUrl":"https://doi.org/10.1111/tpj.17096","url":null,"abstract":"<p><p>Nourishing the embryo with endosperm and enclosing both embryo and endosperm in the seed coat are two important evolutionary innovations. Seed coat is conventionally viewed as a protective layer that functions after the seed has matured. Here, we challenge this notion by showing that a subregion of the seed coat, termed the chalazal seed coat (CZSC), is geared to gate seed nutrition loading in developing seeds. The CZSC develops the coordinative system comprising the apoplastic isolation, mediated by the restricted suberization, and the active transport, mediated by the specific expression of a variety of transporters, at as early as the globular embryo stage in both Arabidopsis and soybean seeds. This coordinated system in the CZSC disrupts the vascular continuum to the maternal tissues and forces the nutrient transport into selective and active absorption. We further reveal that the precision of the spatiotemporal suberin deposition and transporter expression is controlled by the regulatory hierarchy of SHR-MYBs cascades. Our results provide a mechanistic insight into the assimilate accumulation in dicot seeds.</p>","PeriodicalId":233,"journal":{"name":"The Plant Journal","volume":null,"pages":null},"PeriodicalIF":6.2,"publicationDate":"2024-10-30","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142542441","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}
Maxwell A Ware, Andrew J Paton, Yu Bai, Tessema Kassaw, Martin Lohr, Graham Peers
Algae such as diatoms and haptophytes have distinct photosynthetic pigments from plants, including a novel set of carotenoids. This includes a primary xanthophyll cycle comprised of diadinoxanthin and its de-epoxidation product diatoxanthin that enables the switch between light harvesting and non-photochemical quenching (NPQ)-mediated dissipation of light energy. The enzyme responsible for the reversal of this cycle was previously unknown. Here, we identified zeaxanthin epoxidase 3 (ZEP3) from Phaeodactylum tricornutum as the candidate diatoxanthin epoxidase. Knocking out the ZEP3 gene caused a loss of rapidly reversible NPQ following saturating light exposure. This correlated with the maintenance of high concentrations of diatoxanthin during recovery in low light. Xanthophyll cycling and NPQ relaxation were restored via complementation of the wild-type ZEP3 gene. The zep3 knockout strains showed reduced photosynthetic rates at higher light fluxes and reduced specific growth rate in variable light regimes, likely due to the mutant strains becoming locked in a light energy dissipation state. We were able to toggle the level of NPQ capacity in a time and dose dependent manner by placing the ZEP3 gene under the control of a β-estradiol inducible promoter. Identification of this gene provides a deeper understanding of the diversification of photosynthetic control in algae compared to plants and suggests a potential target to improve the productivity of industrial-scale cultures.
{"title":"Identifying the gene responsible for non-photochemical quenching reversal in Phaeodactylum tricornutum.","authors":"Maxwell A Ware, Andrew J Paton, Yu Bai, Tessema Kassaw, Martin Lohr, Graham Peers","doi":"10.1111/tpj.17104","DOIUrl":"https://doi.org/10.1111/tpj.17104","url":null,"abstract":"<p><p>Algae such as diatoms and haptophytes have distinct photosynthetic pigments from plants, including a novel set of carotenoids. This includes a primary xanthophyll cycle comprised of diadinoxanthin and its de-epoxidation product diatoxanthin that enables the switch between light harvesting and non-photochemical quenching (NPQ)-mediated dissipation of light energy. The enzyme responsible for the reversal of this cycle was previously unknown. Here, we identified zeaxanthin epoxidase 3 (ZEP3) from Phaeodactylum tricornutum as the candidate diatoxanthin epoxidase. Knocking out the ZEP3 gene caused a loss of rapidly reversible NPQ following saturating light exposure. This correlated with the maintenance of high concentrations of diatoxanthin during recovery in low light. Xanthophyll cycling and NPQ relaxation were restored via complementation of the wild-type ZEP3 gene. The zep3 knockout strains showed reduced photosynthetic rates at higher light fluxes and reduced specific growth rate in variable light regimes, likely due to the mutant strains becoming locked in a light energy dissipation state. We were able to toggle the level of NPQ capacity in a time and dose dependent manner by placing the ZEP3 gene under the control of a β-estradiol inducible promoter. Identification of this gene provides a deeper understanding of the diversification of photosynthetic control in algae compared to plants and suggests a potential target to improve the productivity of industrial-scale cultures.</p>","PeriodicalId":233,"journal":{"name":"The Plant Journal","volume":null,"pages":null},"PeriodicalIF":6.2,"publicationDate":"2024-10-30","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142542439","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}
Cui-Hong Hao, Chen Pang, Li-Na Yang, Feng Xiong, Sha Li
Dormancy is an essential characteristic that enables seeds to survive in unfavorable conditions while germinating when conditions are favorable. Myosin-binding proteins (MyoBs) assist in the movement of organelles along actin microfilaments by attaching to both organelles and myosins. In contrast to studies on yeast and metazoans, research on plant MyoBs is still in its early stages and primarily focuses on tip-growing cells. In this study, we found that Arabidopsis MyoB13 is highly expressed in dry mature seeds. The myob13 mutant, created using CRISPR/Cas9, exhibits a preharvest sprouting phenotype, which can be mitigated by after-ripening treatment, indicating that MyoB13 plays a positive role in primary seed dormancy. Furthermore, we show that MyoB13 negatively regulates ABA biosynthesis and signaling pathways. Notably, the expression of MyoB13 orthologs from maize and soybean can completely restore the phenotype of the Arabidopsis myob13 mutant, suggesting that the function of MyoB13 in ABA-induced seed dormancy is evolutionarily conserved. Therefore, the functional characterization of MyoB13 offers an additional genetic resource to help prevent vivipary in crop species.
休眠是种子能够在不利条件下存活并在有利条件下萌发的一个基本特征。肌球蛋白结合蛋白(MyoBs)通过附着在细胞器和肌球蛋白上,帮助细胞器沿着肌动蛋白微丝运动。与对酵母和元气动物的研究不同,对植物 MyoBs 的研究仍处于早期阶段,主要集中在顶端生长细胞。在这项研究中,我们发现拟南芥 MyoB13 在干燥成熟的种子中高度表达。利用CRISPR/Cas9技术创建的myob13突变体表现出收获前萌发的表型,这种表型可以通过后熟处理得到缓解,这表明MyoB13在初级种子休眠中发挥着积极作用。此外,我们还发现 MyoB13 负向调节 ABA 的生物合成和信号通路。值得注意的是,表达玉米和大豆的 MyoB13 同源物可以完全恢复拟南芥 myob13 突变体的表型,这表明 MyoB13 在 ABA 诱导的种子休眠中的功能在进化上是保守的。因此,MyoB13的功能特征描述为帮助作物物种防止胎生提供了额外的遗传资源。
{"title":"Myosin-binding protein 13 mediates primary seed dormancy via abscisic acid biosynthesis and signaling in Arabidopsis.","authors":"Cui-Hong Hao, Chen Pang, Li-Na Yang, Feng Xiong, Sha Li","doi":"10.1111/tpj.17112","DOIUrl":"https://doi.org/10.1111/tpj.17112","url":null,"abstract":"<p><p>Dormancy is an essential characteristic that enables seeds to survive in unfavorable conditions while germinating when conditions are favorable. Myosin-binding proteins (MyoBs) assist in the movement of organelles along actin microfilaments by attaching to both organelles and myosins. In contrast to studies on yeast and metazoans, research on plant MyoBs is still in its early stages and primarily focuses on tip-growing cells. In this study, we found that Arabidopsis MyoB13 is highly expressed in dry mature seeds. The myob13 mutant, created using CRISPR/Cas9, exhibits a preharvest sprouting phenotype, which can be mitigated by after-ripening treatment, indicating that MyoB13 plays a positive role in primary seed dormancy. Furthermore, we show that MyoB13 negatively regulates ABA biosynthesis and signaling pathways. Notably, the expression of MyoB13 orthologs from maize and soybean can completely restore the phenotype of the Arabidopsis myob13 mutant, suggesting that the function of MyoB13 in ABA-induced seed dormancy is evolutionarily conserved. Therefore, the functional characterization of MyoB13 offers an additional genetic resource to help prevent vivipary in crop species.</p>","PeriodicalId":233,"journal":{"name":"The Plant Journal","volume":null,"pages":null},"PeriodicalIF":6.2,"publicationDate":"2024-10-30","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142542440","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}
Bárbara Baesso Moura, Yasutomo Hoshika, Cecilia Brunetti, Luana Beatriz Dos Santos Nascimento, Elena Marra, Elena Paoletti, Francesco Ferrini
Ozone (O3) is an oxidative pollutant that significantly threatens plant development and ecological dynamics. The present study explores the impact of O3 on Moringa (Moringa oleifera) ecotypes when exposed to ambient and elevated O3 levels. Elevated O3 concentrations resulted in significant reductions in total biomass for all ecotypes. Photosynthetic parameters, including stomatal conductance (gsto), CO2 assimilation (Pn), and carboxylation efficiency (K), decreased under elevated O3 in some ecotypes, indicating a detrimental effect on carbon assimilation. Nonstructural carbohydrate (NSC) levels in roots varied among ecotypes, with significant reductions in starch content observed under elevated O3, suggesting a potential shift towards soluble sugar accumulation and reallocation for antioxidant defense. Secondary metabolite analysis revealed increased polyphenol production, particularly quercetin derivatives, under elevated O3 in specific ecotypes, highlighting their role in mitigating oxidative stress. Interestingly, the glucosinolate content also varied, with some ecotypes exhibiting increased levels, suggesting a complex regulatory mechanism in response to O3 exposure. The study underscores the intrinsic variability among Moringa ecotypes in response to O3 stress, emphasizing the importance of genetic diversity for adaptation. The findings indicate that Moringa's metabolic plasticity, including shifts in NSC and SM production, plays a crucial role in its defense mechanisms against O3-induced oxidative stress. These insights are vital for optimizing the cultivation and utilization of Moringa in diverse environmental conditions, particularly in regions with elevated O3 levels.
{"title":"Stress physiology of Moringa oleifera under tropospheric ozone enrichment: An ecotype-specific investigation into growth, nonstructural carbohydrates, and polyphenols.","authors":"Bárbara Baesso Moura, Yasutomo Hoshika, Cecilia Brunetti, Luana Beatriz Dos Santos Nascimento, Elena Marra, Elena Paoletti, Francesco Ferrini","doi":"10.1111/tpj.17107","DOIUrl":"https://doi.org/10.1111/tpj.17107","url":null,"abstract":"<p><p>Ozone (O<sub>3</sub>) is an oxidative pollutant that significantly threatens plant development and ecological dynamics. The present study explores the impact of O<sub>3</sub> on Moringa (Moringa oleifera) ecotypes when exposed to ambient and elevated O<sub>3</sub> levels. Elevated O<sub>3</sub> concentrations resulted in significant reductions in total biomass for all ecotypes. Photosynthetic parameters, including stomatal conductance (g<sub>sto</sub>), CO<sub>2</sub> assimilation (P<sub>n</sub>), and carboxylation efficiency (K), decreased under elevated O<sub>3</sub> in some ecotypes, indicating a detrimental effect on carbon assimilation. Nonstructural carbohydrate (NSC) levels in roots varied among ecotypes, with significant reductions in starch content observed under elevated O<sub>3</sub>, suggesting a potential shift towards soluble sugar accumulation and reallocation for antioxidant defense. Secondary metabolite analysis revealed increased polyphenol production, particularly quercetin derivatives, under elevated O<sub>3</sub> in specific ecotypes, highlighting their role in mitigating oxidative stress. Interestingly, the glucosinolate content also varied, with some ecotypes exhibiting increased levels, suggesting a complex regulatory mechanism in response to O<sub>3</sub> exposure. The study underscores the intrinsic variability among Moringa ecotypes in response to O<sub>3</sub> stress, emphasizing the importance of genetic diversity for adaptation. The findings indicate that Moringa's metabolic plasticity, including shifts in NSC and SM production, plays a crucial role in its defense mechanisms against O<sub>3</sub>-induced oxidative stress. These insights are vital for optimizing the cultivation and utilization of Moringa in diverse environmental conditions, particularly in regions with elevated O<sub>3</sub> levels.</p>","PeriodicalId":233,"journal":{"name":"The Plant Journal","volume":null,"pages":null},"PeriodicalIF":6.2,"publicationDate":"2024-10-30","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142542442","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}
Plants direct substantial amounts of carbon toward the biosynthesis of aromatic amino acids (AAAs), particularly phenylalanine to produce lignin and other phenylpropanoids. Yet, we have a limited understanding of how plants regulate AAA metabolism, partially because of a scarcity of robust analytical methods. Here, we established a simplified workflow for simultaneous quantification of AAAs and their pathway intermediates from plant tissues, based on extraction at two alternative pH and analysis by Zwitterionic hydrophilic interaction liquid chromatography coupled to mass spectrometry. This workflow was then used to analyze metabolic responses to elevated or reduced carbon flow through the shikimate pathway in plants. Increased flow upon expression of a feedback-insensitive isoform of the first shikimate pathway enzyme elevated all AAAs and pathway intermediates, especially arogenate, the last common precursor within the post-chorismate pathway of tyrosine and phenylalanine biosynthesis. Additional overexpression of an arogenate dehydrogenase enzyme increased tyrosine levels and depleted phenylalanine and arogenate pools; however, the upstream shikimate pathway intermediates remained accumulated at high levels. Glyphosate treatment, which restricts carbon flow through the shikimate pathway by inhibiting its penultimate step, led to a predictable accumulation of shikimate and other precursors upstream of its target enzyme but also caused an unexpected accumulation of downstream metabolites, including arogenate. These findings highlight that the shikimate pathway and the downstream post-chorismate AAA pathways function as independently regulated modules in plants. The method developed here paves the way for a deeper understanding of the shikimate and AAA biosynthetic pathways in plants.
{"title":"A simplified liquid chromatography-mass spectrometry methodology to probe the shikimate and aromatic amino acid biosynthetic pathways in plants.","authors":"Jorge El-Azaz, Hiroshi A Maeda","doi":"10.1111/tpj.17105","DOIUrl":"https://doi.org/10.1111/tpj.17105","url":null,"abstract":"<p><p>Plants direct substantial amounts of carbon toward the biosynthesis of aromatic amino acids (AAAs), particularly phenylalanine to produce lignin and other phenylpropanoids. Yet, we have a limited understanding of how plants regulate AAA metabolism, partially because of a scarcity of robust analytical methods. Here, we established a simplified workflow for simultaneous quantification of AAAs and their pathway intermediates from plant tissues, based on extraction at two alternative pH and analysis by Zwitterionic hydrophilic interaction liquid chromatography coupled to mass spectrometry. This workflow was then used to analyze metabolic responses to elevated or reduced carbon flow through the shikimate pathway in plants. Increased flow upon expression of a feedback-insensitive isoform of the first shikimate pathway enzyme elevated all AAAs and pathway intermediates, especially arogenate, the last common precursor within the post-chorismate pathway of tyrosine and phenylalanine biosynthesis. Additional overexpression of an arogenate dehydrogenase enzyme increased tyrosine levels and depleted phenylalanine and arogenate pools; however, the upstream shikimate pathway intermediates remained accumulated at high levels. Glyphosate treatment, which restricts carbon flow through the shikimate pathway by inhibiting its penultimate step, led to a predictable accumulation of shikimate and other precursors upstream of its target enzyme but also caused an unexpected accumulation of downstream metabolites, including arogenate. These findings highlight that the shikimate pathway and the downstream post-chorismate AAA pathways function as independently regulated modules in plants. The method developed here paves the way for a deeper understanding of the shikimate and AAA biosynthetic pathways in plants.</p>","PeriodicalId":233,"journal":{"name":"The Plant Journal","volume":null,"pages":null},"PeriodicalIF":6.2,"publicationDate":"2024-10-28","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142520564","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}
Athanas Guzha, Barsanti Gautam, Damiano Marchiafava, Julius Ver Sagun, Tatiana Garcia, Brice A Jarvis, Allison M Barbaglia-Hurlock, Christopher Johnston, Erich Grotewold, John C Sedbrook, Ana Paula Alonso, Kent D Chapman
Lipid droplets (LDs) are unusual organelles that have a phospholipid monolayer surface and a hydrophobic matrix. In oilseeds, this matrix is nearly always composed of triacylglycerols (TGs) for efficient storage of carbon and energy. Various proteins play a role in their assembly, stability and turnover, and even though the major structural oleosin proteins in seed LDs have been known for decades, the factors influencing LD formation and dynamics are still being uncovered mostly in the "model oilseed" Arabidopsis. Here we identified several key LD biogenesis proteins in the seeds of pennycress, a potential biofuel crop, that were correlated previously with seed oil content and characterized here for their participation in LD formation in transient expression assays and stable transgenics. One pennycress protein, the lipid droplet associated protein-interacting protein (LDIP), was able to functionally complement the Arabidopsis ldip mutant, emphasizing the close conservation of lipid storage among these two Brassicas. Moreover, loss-of-function ldip mutants in pennycress exhibited increased seed oil content without compromising plant growth, raising the possibility that LDIP or other LD biogenesis factors may be suitable targets for improving yields in oilseed crops more broadly.
{"title":"Targeted modulation of pennycress lipid droplet proteins impacts droplet morphology and seed oil content.","authors":"Athanas Guzha, Barsanti Gautam, Damiano Marchiafava, Julius Ver Sagun, Tatiana Garcia, Brice A Jarvis, Allison M Barbaglia-Hurlock, Christopher Johnston, Erich Grotewold, John C Sedbrook, Ana Paula Alonso, Kent D Chapman","doi":"10.1111/tpj.17109","DOIUrl":"https://doi.org/10.1111/tpj.17109","url":null,"abstract":"<p><p>Lipid droplets (LDs) are unusual organelles that have a phospholipid monolayer surface and a hydrophobic matrix. In oilseeds, this matrix is nearly always composed of triacylglycerols (TGs) for efficient storage of carbon and energy. Various proteins play a role in their assembly, stability and turnover, and even though the major structural oleosin proteins in seed LDs have been known for decades, the factors influencing LD formation and dynamics are still being uncovered mostly in the \"model oilseed\" Arabidopsis. Here we identified several key LD biogenesis proteins in the seeds of pennycress, a potential biofuel crop, that were correlated previously with seed oil content and characterized here for their participation in LD formation in transient expression assays and stable transgenics. One pennycress protein, the lipid droplet associated protein-interacting protein (LDIP), was able to functionally complement the Arabidopsis ldip mutant, emphasizing the close conservation of lipid storage among these two Brassicas. Moreover, loss-of-function ldip mutants in pennycress exhibited increased seed oil content without compromising plant growth, raising the possibility that LDIP or other LD biogenesis factors may be suitable targets for improving yields in oilseed crops more broadly.</p>","PeriodicalId":233,"journal":{"name":"The Plant Journal","volume":null,"pages":null},"PeriodicalIF":6.2,"publicationDate":"2024-10-28","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142520566","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}
Land plants have evolved a hydrophobic cuticle on the surface of aerial organs as an adaptation to ensure survival in terrestrial environments. Cuticle is mainly composed of lipids, namely cutin and intracuticular wax, with epicuticular wax deposited on plant surface. The composition and permeability of cuticle have a large influence on its ability to protect plants against drought stress. However, the regulatory mechanisms underlying cuticular wax biosynthesis in response to drought stress have not been fully elucidated. Here, we identified three AP2/ERF transcription factors (DREB26/ERF12, ERF13 and ERF14) involved in the regulation of water permeability of the plant surface. Transmission electron microscopy revealed thicker cuticle on the leaves of DREB26-overexpressing (DREB26OX) plants, and thinner cuticle on the leaves of transgenic plants expressing SRDX repression domain-fused DREB26 (DREB26SR). Genes involved in cuticular wax formation were upregulated in DREB26OX and downregulated in DREB26SR. The levels of very-long chain (VLC) alkanes, which are a major wax component, increased in DREB26OX leaves and decreased in DREB26SR leaves. Under dehydration stress, water loss was reduced in DREB26OX and increased in DREB26SR. The erf12/13/14 triple mutant showed delayed growth, decreased leaf water content, and reduced drought-inducible VLC alkane accumulation. Taken together, our results indicate that the DREB26/ERF12 and its closed family members, ERF13 and ERF14, play an important role in cuticular wax biosynthesis in response to drought stress. The complex transcriptional cascade involved in the regulation of cuticular wax biosynthesis under drought stress conditions is discussed.
{"title":"Arabidopsis DREB26/ERF12 and its close relatives regulate cuticular wax biosynthesis under drought stress condition.","authors":"Kaoru Urano, Yoshimi Oshima, Toshiki Ishikawa, Takuma Kajino, Shingo Sakamoto, Mayuko Sato, Kiminori Toyooka, Miki Fujita, Maki Kawai-Yamada, Teruaki Taji, Kyonoshin Maruyama, Kazuko Yamaguchi-Shinozaki, Kazuo Shinozaki","doi":"10.1111/tpj.17100","DOIUrl":"https://doi.org/10.1111/tpj.17100","url":null,"abstract":"<p><p>Land plants have evolved a hydrophobic cuticle on the surface of aerial organs as an adaptation to ensure survival in terrestrial environments. Cuticle is mainly composed of lipids, namely cutin and intracuticular wax, with epicuticular wax deposited on plant surface. The composition and permeability of cuticle have a large influence on its ability to protect plants against drought stress. However, the regulatory mechanisms underlying cuticular wax biosynthesis in response to drought stress have not been fully elucidated. Here, we identified three AP2/ERF transcription factors (DREB26/ERF12, ERF13 and ERF14) involved in the regulation of water permeability of the plant surface. Transmission electron microscopy revealed thicker cuticle on the leaves of DREB26-overexpressing (DREB26OX) plants, and thinner cuticle on the leaves of transgenic plants expressing SRDX repression domain-fused DREB26 (DREB26SR). Genes involved in cuticular wax formation were upregulated in DREB26OX and downregulated in DREB26SR. The levels of very-long chain (VLC) alkanes, which are a major wax component, increased in DREB26OX leaves and decreased in DREB26SR leaves. Under dehydration stress, water loss was reduced in DREB26OX and increased in DREB26SR. The erf12/13/14 triple mutant showed delayed growth, decreased leaf water content, and reduced drought-inducible VLC alkane accumulation. Taken together, our results indicate that the DREB26/ERF12 and its closed family members, ERF13 and ERF14, play an important role in cuticular wax biosynthesis in response to drought stress. The complex transcriptional cascade involved in the regulation of cuticular wax biosynthesis under drought stress conditions is discussed.</p>","PeriodicalId":233,"journal":{"name":"The Plant Journal","volume":null,"pages":null},"PeriodicalIF":6.2,"publicationDate":"2024-10-28","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142520565","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}
Previous research on the ripening process of many fruit crop varieties typically involved analyses of the conserved genetic factors among species. However, even for seemingly identical ripening processes, the associated gene expression networks often evolved independently, as reflected by the diversity in the interactions between transcription factors (TFs) and the targeted cis-regulatory elements (CREs). In this study, explainable deep learning (DL) frameworks were used to predict expression patterns on the basis of CREs in promoter sequences. We initially screened potential lineage-specific CRE-TF interactions influencing the kiwifruit ripening process, which is triggered by ethylene, similar to the corresponding processes in other climacteric fruit crops. Some novel regulatory relationships affecting ethylene-induced fruit ripening were identified. Specifically, ABI5-like bZIP, G2-like, and MYB81-like TFs were revealed as trans-factors modulating the expression of representative ethylene signaling/biosynthesis-related genes (e.g., ACS1, ERT2, and ERF143). Transient reporter assays and DNA affinity purification sequencing (DAP-Seq) analyses validated these CRE-TF interactions and their regulatory relationships. A comparative analysis with co-expression networking suggested that this DL-based screening can identify regulatory networks independently of co-expression patterns. Our results highlight the utility of an explainable DL approach for identifying novel CRE-TF interactions. These imply that fruit crop species may have evolved lineage-specific fruit ripening-related cis-trans regulatory networks.
{"title":"Identification of lineage-specific cis-trans regulatory networks related to kiwifruit ripening initiation.","authors":"Eriko Kuwada, Kouki Takeshita, Taiji Kawakatsu, Seiichi Uchida, Takashi Akagi","doi":"10.1111/tpj.17093","DOIUrl":"https://doi.org/10.1111/tpj.17093","url":null,"abstract":"<p><p>Previous research on the ripening process of many fruit crop varieties typically involved analyses of the conserved genetic factors among species. However, even for seemingly identical ripening processes, the associated gene expression networks often evolved independently, as reflected by the diversity in the interactions between transcription factors (TFs) and the targeted cis-regulatory elements (CREs). In this study, explainable deep learning (DL) frameworks were used to predict expression patterns on the basis of CREs in promoter sequences. We initially screened potential lineage-specific CRE-TF interactions influencing the kiwifruit ripening process, which is triggered by ethylene, similar to the corresponding processes in other climacteric fruit crops. Some novel regulatory relationships affecting ethylene-induced fruit ripening were identified. Specifically, ABI5-like bZIP, G2-like, and MYB81-like TFs were revealed as trans-factors modulating the expression of representative ethylene signaling/biosynthesis-related genes (e.g., ACS1, ERT2, and ERF143). Transient reporter assays and DNA affinity purification sequencing (DAP-Seq) analyses validated these CRE-TF interactions and their regulatory relationships. A comparative analysis with co-expression networking suggested that this DL-based screening can identify regulatory networks independently of co-expression patterns. Our results highlight the utility of an explainable DL approach for identifying novel CRE-TF interactions. These imply that fruit crop species may have evolved lineage-specific fruit ripening-related cis-trans regulatory networks.</p>","PeriodicalId":233,"journal":{"name":"The Plant Journal","volume":null,"pages":null},"PeriodicalIF":6.2,"publicationDate":"2024-10-27","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142491823","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}
Dorothy D Sweet, Sara B Tirado, Julian Cooper, Nathan M Springer, Cory D Hirsch, Candice N Hirsch
Plant height can be an indicator of plant health across environments and used to identify superior genotypes. Typically plant height is measured at a single timepoint when plants reach terminal height. Evaluating plant height using unoccupied aerial vehicles allows for measurements throughout the growing season, facilitating a better understanding of plant-environment interactions and the genetic basis of this complex trait. To assess variation throughout development, plant height data was collected from planting until terminal height at anthesis (14 flights 2018, 27 in 2019, 12 in 2020, and 11 in 2021) for a panel of ~500 diverse maize inbred lines. The percent variance explained in plant height throughout the season was significantly explained by genotype (9-48%), year (4-52%), and genotype-by-year interactions (14-36%) to varying extents throughout development. Genome-wide association studies revealed 717 significant single nucleotide polymorphisms associated with plant height and growth rate at different parts of the growing season specific to certain phases of vegetative growth. When plant height growth curves were compared to growth curves estimated from canopy cover, greater Fréchet distance stability was observed in plant height growth curves than for canopy cover. This indicated canopy cover may be more useful for understanding environmental modulation of overall plant growth and plant height better for understanding genotypic modulation of overall plant growth. This study demonstrated that substantial information can be gained from high temporal resolution data to understand how plants differentially interact with the environment and can enhance our understanding of the genetic basis of complex polygenic traits.
{"title":"Temporally resolved growth patterns reveal novel information about the polygenic nature of complex quantitative traits.","authors":"Dorothy D Sweet, Sara B Tirado, Julian Cooper, Nathan M Springer, Cory D Hirsch, Candice N Hirsch","doi":"10.1111/tpj.17092","DOIUrl":"https://doi.org/10.1111/tpj.17092","url":null,"abstract":"<p><p>Plant height can be an indicator of plant health across environments and used to identify superior genotypes. Typically plant height is measured at a single timepoint when plants reach terminal height. Evaluating plant height using unoccupied aerial vehicles allows for measurements throughout the growing season, facilitating a better understanding of plant-environment interactions and the genetic basis of this complex trait. To assess variation throughout development, plant height data was collected from planting until terminal height at anthesis (14 flights 2018, 27 in 2019, 12 in 2020, and 11 in 2021) for a panel of ~500 diverse maize inbred lines. The percent variance explained in plant height throughout the season was significantly explained by genotype (9-48%), year (4-52%), and genotype-by-year interactions (14-36%) to varying extents throughout development. Genome-wide association studies revealed 717 significant single nucleotide polymorphisms associated with plant height and growth rate at different parts of the growing season specific to certain phases of vegetative growth. When plant height growth curves were compared to growth curves estimated from canopy cover, greater Fréchet distance stability was observed in plant height growth curves than for canopy cover. This indicated canopy cover may be more useful for understanding environmental modulation of overall plant growth and plant height better for understanding genotypic modulation of overall plant growth. This study demonstrated that substantial information can be gained from high temporal resolution data to understand how plants differentially interact with the environment and can enhance our understanding of the genetic basis of complex polygenic traits.</p>","PeriodicalId":233,"journal":{"name":"The Plant Journal","volume":null,"pages":null},"PeriodicalIF":6.2,"publicationDate":"2024-10-27","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142491828","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}
Katja Stojkovič, Camilla Canovi, Kim-Cuong Le, Iftikhar Ahmad, Ioana Gaboreanu, Sofie Johansson, Nicolas Delhomme, Ulrika Egertsdotter, Nathaniel R Street
Somatic embryogenesis (SE) is a powerful model system for studying embryo development and an important method for scaling up availability of elite and climate-adapted genetic material of Norway spruce (Picea abies L. Karst). However, there are several steps during the development of the somatic embryo (Sem) that are suboptimal compared to zygotic embryo (Zem) development. These differences are poorly understood and result in substantial yield losses during plant production, which limits cost-effective large-scale production of SE plants. This study presents a comprehensive data resource profiling gene expression during zygotic and somatic embryo development to support studies aiming to advance understanding of gene regulatory programmes controlling embryo development. Transcriptome expression patterns were analysed during zygotic embryogenesis (ZE) in Norway spruce, including separated samples of the female gametophytes and Zem, and at multiple stages during SE. Expression data from eight developmental stages of SE, starting with pro-embryogenic masses (PEMs) up until germination, revealed extensive modulation of the transcriptome between the early and mid-stage maturing embryos and at the transition of desiccated embryos to germination. Comparative analysis of gene expression changes during ZE and SE identified differences in the pattern of gene expression changes and functional enrichment of these provided insight into the associated biological processes. Orthologs of transcription factors known to regulate embryo development in angiosperms were differentially regulated during Zem and Sem development and in the different zygotic embryo tissues, providing clues to the differences in development observed between Zem and Sem. This resource represents the most comprehensive dataset available for exploring embryo development in conifers.
体细胞胚胎发生(SE)是研究胚胎发育的强大模型系统,也是扩大挪威云杉(Picea abies L. Karst)精英和气候适应性遗传材料可用性的重要方法。然而,在体细胞胚胎(Sem)的发育过程中,有几个步骤与子代胚胎(Zem)的发育相比并不理想。人们对这些差异知之甚少,因此在植物生产过程中造成了巨大的产量损失,限制了 SE 植物经济高效的大规模生产。本研究提供了一个全面的数据资源,分析了合子胚和体细胞胚发育过程中的基因表达,以支持旨在促进对控制胚发育的基因调控程序的了解的研究。研究人员分析了挪威云杉子代胚胎发生(ZE)过程中的转录组表达模式,包括雌配子体和Zem的分离样本,以及SE过程中多个阶段的转录组表达模式。从原胚胎块(PEM)开始直至萌芽的八个发育阶段的表达数据显示,转录组在早期和中期成熟胚胎之间以及在干燥胚胎向萌芽的过渡阶段发生了广泛的变化。对ZE和SE期间基因表达变化的比较分析发现了基因表达变化模式的差异,对这些差异的功能富集有助于深入了解相关的生物过程。已知调控被子植物胚胎发育的转录因子的同源物在Zem和Sem发育过程中以及在不同的合子胚胎组织中受到不同的调控,从而为观察到Zem和Sem发育过程中的差异提供了线索。该资源是目前可用于探索针叶树胚胎发育的最全面的数据集。
{"title":"A transcriptome atlas of zygotic and somatic embryogenesis in Norway spruce.","authors":"Katja Stojkovič, Camilla Canovi, Kim-Cuong Le, Iftikhar Ahmad, Ioana Gaboreanu, Sofie Johansson, Nicolas Delhomme, Ulrika Egertsdotter, Nathaniel R Street","doi":"10.1111/tpj.17087","DOIUrl":"https://doi.org/10.1111/tpj.17087","url":null,"abstract":"<p><p>Somatic embryogenesis (SE) is a powerful model system for studying embryo development and an important method for scaling up availability of elite and climate-adapted genetic material of Norway spruce (Picea abies L. Karst). However, there are several steps during the development of the somatic embryo (Sem) that are suboptimal compared to zygotic embryo (Zem) development. These differences are poorly understood and result in substantial yield losses during plant production, which limits cost-effective large-scale production of SE plants. This study presents a comprehensive data resource profiling gene expression during zygotic and somatic embryo development to support studies aiming to advance understanding of gene regulatory programmes controlling embryo development. Transcriptome expression patterns were analysed during zygotic embryogenesis (ZE) in Norway spruce, including separated samples of the female gametophytes and Zem, and at multiple stages during SE. Expression data from eight developmental stages of SE, starting with pro-embryogenic masses (PEMs) up until germination, revealed extensive modulation of the transcriptome between the early and mid-stage maturing embryos and at the transition of desiccated embryos to germination. Comparative analysis of gene expression changes during ZE and SE identified differences in the pattern of gene expression changes and functional enrichment of these provided insight into the associated biological processes. Orthologs of transcription factors known to regulate embryo development in angiosperms were differentially regulated during Zem and Sem development and in the different zygotic embryo tissues, providing clues to the differences in development observed between Zem and Sem. This resource represents the most comprehensive dataset available for exploring embryo development in conifers.</p>","PeriodicalId":233,"journal":{"name":"The Plant Journal","volume":null,"pages":null},"PeriodicalIF":6.2,"publicationDate":"2024-10-27","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142491802","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}