Dioscorea alata, a key tuber crop for global food security, is threatened by anthracnose disease caused by Colletotrichum gloeosporioides. However, identification of functional resistance genes against C. gloeosporioides in D. alata is challenging due to low flowering and hybridization efficiency of this plant. Nucleotide-binding leucine-rich repeat (NLR) genes constitute the largest group of plant disease resistance genes, from which functional genes against diverse pathogens across various crops have been cloned. In this study, a comprehensive genome-wide analysis identified 346 NLR genes from D. alata, including one RNL and 345 CNLs. These NLRs were unequally distributed on 20 chromosomes, with chromosome 3 harboring the highest number (78 NLR genes). The majority of NLR genes (91%) were located in multigene clusters, implying that tandem or proximal duplication was the primary driving force for NLR gene expansion in D. alata. Comparative analysis of Dioscoreaceae species revealed high variability and differential expansion patterns of NLR genes. In addition, transcriptome profiling of D. alata post-infection with C. gloeosporioides identified 12 differentially expressed NLR genes. In summary, this study sheds new light on the genetic architecture and evolutionary dynamics of D. alata NLR genes, offering valuable insights for cloning functional genes against C. gloeosporioides.
{"title":"Deciphering the landscape and evolutionary trajectory of NLR immune receptors in Dioscorea alata.","authors":"Yue Wang, Xing-Yu Feng, Wen-Qiang Wu, Ming-Han Li, Sai-Xi Li, Zhen Zeng, Zhu-Qing Shao, Yan-Mei Zhang","doi":"10.1007/s11103-024-01541-x","DOIUrl":"10.1007/s11103-024-01541-x","url":null,"abstract":"<p><p>Dioscorea alata, a key tuber crop for global food security, is threatened by anthracnose disease caused by Colletotrichum gloeosporioides. However, identification of functional resistance genes against C. gloeosporioides in D. alata is challenging due to low flowering and hybridization efficiency of this plant. Nucleotide-binding leucine-rich repeat (NLR) genes constitute the largest group of plant disease resistance genes, from which functional genes against diverse pathogens across various crops have been cloned. In this study, a comprehensive genome-wide analysis identified 346 NLR genes from D. alata, including one RNL and 345 CNLs. These NLRs were unequally distributed on 20 chromosomes, with chromosome 3 harboring the highest number (78 NLR genes). The majority of NLR genes (91%) were located in multigene clusters, implying that tandem or proximal duplication was the primary driving force for NLR gene expansion in D. alata. Comparative analysis of Dioscoreaceae species revealed high variability and differential expansion patterns of NLR genes. In addition, transcriptome profiling of D. alata post-infection with C. gloeosporioides identified 12 differentially expressed NLR genes. In summary, this study sheds new light on the genetic architecture and evolutionary dynamics of D. alata NLR genes, offering valuable insights for cloning functional genes against C. gloeosporioides.</p>","PeriodicalId":20064,"journal":{"name":"Plant Molecular Biology","volume":"115 1","pages":"13"},"PeriodicalIF":3.9,"publicationDate":"2024-12-25","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142886036","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}
Pub Date : 2024-12-24DOI: 10.1007/s11103-024-01535-9
Jing Cui, Chuanghao Li, Jin Qi, Wenjin Yu, Changxia Li
Cold stress is an environmental factor that seriously restricts the growth, production and survival of plants, and has received extensive attention in recent years. Hydrogen sulfide (H2S) is an ubiquitous gas signaling molecule, and its role in alleviating plant cold stress has become a research focus in recent years. This paper reviews for the first time the significant effect of H2S on improving plant cold resistance, which makes up for the gaps in the existing literature. In general, H2S improves plant tolerance to cold stress by activating antioxidant reaction and promoting the accumulation of metabolic substances such as chlorophyll, flavonoids, proline, sucrose and total soluble sugar in plants. Interestingly, H2S also interacts with nitric oxide (NO), auxin, jasmonic acid (JA), salicylic acid (SA), and ethylene (ETH) to alleviate cold stress. More importantly, in the process of alleviating cold stress with H2S, gene expression related to H2S synthesis, cold response and antioxidant is up-regulated or down-regulated, leading to the improvement of plant cold resistance. This paper also points out the problems existing in the current research and the potential of H2S in agricultural practice, and provides relevant theoretical references for future research in this field.
{"title":"Hydrogen sulfide in plant cold stress: functions, mechanisms, and challenge.","authors":"Jing Cui, Chuanghao Li, Jin Qi, Wenjin Yu, Changxia Li","doi":"10.1007/s11103-024-01535-9","DOIUrl":"10.1007/s11103-024-01535-9","url":null,"abstract":"<p><p>Cold stress is an environmental factor that seriously restricts the growth, production and survival of plants, and has received extensive attention in recent years. Hydrogen sulfide (H<sub>2</sub>S) is an ubiquitous gas signaling molecule, and its role in alleviating plant cold stress has become a research focus in recent years. This paper reviews for the first time the significant effect of H<sub>2</sub>S on improving plant cold resistance, which makes up for the gaps in the existing literature. In general, H<sub>2</sub>S improves plant tolerance to cold stress by activating antioxidant reaction and promoting the accumulation of metabolic substances such as chlorophyll, flavonoids, proline, sucrose and total soluble sugar in plants. Interestingly, H<sub>2</sub>S also interacts with nitric oxide (NO), auxin, jasmonic acid (JA), salicylic acid (SA), and ethylene (ETH) to alleviate cold stress. More importantly, in the process of alleviating cold stress with H<sub>2</sub>S, gene expression related to H<sub>2</sub>S synthesis, cold response and antioxidant is up-regulated or down-regulated, leading to the improvement of plant cold resistance. This paper also points out the problems existing in the current research and the potential of H<sub>2</sub>S in agricultural practice, and provides relevant theoretical references for future research in this field.</p>","PeriodicalId":20064,"journal":{"name":"Plant Molecular Biology","volume":"115 1","pages":"12"},"PeriodicalIF":3.9,"publicationDate":"2024-12-24","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142882487","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}
Plant lipid transfer proteins (LTPs) are distinguished by their capacity to facilitate lipid transport in vitro between membranes. This includes the transportation of lipid constituents from the tapetum to the microspore, thereby playing a pivotal role in the synthesis and construction of the pollen wall, encompassing the formation of the pollen aperture. However, our understanding of LTPs and their role in pollen aperture formation in rice remains limited. In this study, we have isolated and characterized a male sterile rice mutant named as pollen aperture defect 1 (Ospad1). When compared to the wild type, Ospad1 mutant plants exhibit pollen grain abortion due to the absence of the fibrillar-granular layer, ultimately leading to the leakage of contents from the malformed aperture. OsPAD1 encodes a non-specific LTP and is specifically expressed in the microspore during male development. Subsequently, in vitro lipid binding assays reveal that the recombinant OsPAD1 protein has the capability to bind to a broad spectrum of lipids. The malfunction of OsPAD1 results in disrupted lipid metabolism and compromised pollen aperture, ultimately leading to male sterility. Furthermore, yeast two-hybrid, bimolecular fluorescent complementation and pull-down assays all demonstrate that OsPAD1 can directly interact with OsINP1, an orthologue of a crucial aperture factor in Arabidopsis, together regulating rice aperture development. These findings offer new insights into the molecular mechanisms that underlie the function of LTPs in rice pollen aperture formation. This research holds potential implications not only for rice but also for other cereal crops.
{"title":"OsPAD1, encoding a non-specific lipid transfer protein, is required for rice pollen aperture formation.","authors":"Qiming Wang, Yunlu Tian, Keyi Chen, Shanshan Zhu, Yehui Xiong, Chaolong Wang, Xiaowen Yu, Wenting Bai, Hai Zheng, Shimin You, Yang Hu, Dekun Lei, Anqi Jian, Jiayu Lu, Hao Yu, Xin Zhang, Yulong Ren, Cailin Lei, ZhiJun Cheng, Qibing Lin, Ling Jiang, Zhigang Zhao, Jianmin Wan","doi":"10.1007/s11103-024-01531-z","DOIUrl":"10.1007/s11103-024-01531-z","url":null,"abstract":"<p><p>Plant lipid transfer proteins (LTPs) are distinguished by their capacity to facilitate lipid transport in vitro between membranes. This includes the transportation of lipid constituents from the tapetum to the microspore, thereby playing a pivotal role in the synthesis and construction of the pollen wall, encompassing the formation of the pollen aperture. However, our understanding of LTPs and their role in pollen aperture formation in rice remains limited. In this study, we have isolated and characterized a male sterile rice mutant named as pollen aperture defect 1 (Ospad1). When compared to the wild type, Ospad1 mutant plants exhibit pollen grain abortion due to the absence of the fibrillar-granular layer, ultimately leading to the leakage of contents from the malformed aperture. OsPAD1 encodes a non-specific LTP and is specifically expressed in the microspore during male development. Subsequently, in vitro lipid binding assays reveal that the recombinant OsPAD1 protein has the capability to bind to a broad spectrum of lipids. The malfunction of OsPAD1 results in disrupted lipid metabolism and compromised pollen aperture, ultimately leading to male sterility. Furthermore, yeast two-hybrid, bimolecular fluorescent complementation and pull-down assays all demonstrate that OsPAD1 can directly interact with OsINP1, an orthologue of a crucial aperture factor in Arabidopsis, together regulating rice aperture development. These findings offer new insights into the molecular mechanisms that underlie the function of LTPs in rice pollen aperture formation. This research holds potential implications not only for rice but also for other cereal crops.</p>","PeriodicalId":20064,"journal":{"name":"Plant Molecular Biology","volume":"115 1","pages":"11"},"PeriodicalIF":3.9,"publicationDate":"2024-12-22","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142872788","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}
Pub Date : 2024-12-21DOI: 10.1007/s11103-024-01515-z
Ragupathi Nagarajan, Kaviraj Singh Kahlon, Amita Mohan, Kulvinder S Gill
Heat stress affects various components of photosynthetic machinery of which Rubisco activation inhibition due to heat sensitive Rubisco activase (RCA) is the most prominent. Detailed comparison of RCA coding genes identified a tandem duplication event in the grass family lineage where the duplicated genes showed very different evolutionary pattern. One of the two genes showed high level of sequence conservation whereas the second copy, although present only 1.5 kb away, was highly variable among various plant species because of loss of introns, alternative splicing and loss of the last exon coding redox regulated C-terminal extension domain. Gene specific expression analysis, both at the transcription as well as the protein level, showed very different expression pattern of the two RCA copies. Expression of the highly conserved copy was higher under normal plant growing conditions that decreased many folds under heat stress with substantial genotypic variation, but the variable copy showed much higher expression under heat stress conditions across all grass species. The cultivated rice has only one functional gene as the second copy became nonfunctional due to multiple deletions but Oryza brachyantha and Oryza australiensis still have two functional Rca genes. Detailed analysis of the promoter region of the two copies among various plant species showed insertion of several transposable elements harboring heat responsive elements in the heat inducible copy of the gene. The conserved RCA copy of wheat didn't have any transposable insertions whereas in that of maize has one heat shock element and sorghum had two. It would be interesting to study if the higher level of heat stress tolerance observed in sorghum and maize is associated with the differences observed for RCA. Key message This manuscript is reporting a grass family-specific tandem duplication event in RCA genes of cereals. The duplicated copies underwent neo-functionalization to evolve novel function to deal with heat stress. One copy of the tandem duplication maintained a high level of conservation whereas the second copy showed tremendous divergence to evolve species specific function of the gene. Specific function to respond to heat stress likely evolved via the insertion of various heat responsive elements carried by transposable elements.
{"title":"Tandemly duplicated Rubisco activase genes of cereals show differential evolution and response to heat stress.","authors":"Ragupathi Nagarajan, Kaviraj Singh Kahlon, Amita Mohan, Kulvinder S Gill","doi":"10.1007/s11103-024-01515-z","DOIUrl":"10.1007/s11103-024-01515-z","url":null,"abstract":"<p><p>Heat stress affects various components of photosynthetic machinery of which Rubisco activation inhibition due to heat sensitive Rubisco activase (RCA) is the most prominent. Detailed comparison of RCA coding genes identified a tandem duplication event in the grass family lineage where the duplicated genes showed very different evolutionary pattern. One of the two genes showed high level of sequence conservation whereas the second copy, although present only 1.5 kb away, was highly variable among various plant species because of loss of introns, alternative splicing and loss of the last exon coding redox regulated C-terminal extension domain. Gene specific expression analysis, both at the transcription as well as the protein level, showed very different expression pattern of the two RCA copies. Expression of the highly conserved copy was higher under normal plant growing conditions that decreased many folds under heat stress with substantial genotypic variation, but the variable copy showed much higher expression under heat stress conditions across all grass species. The cultivated rice has only one functional gene as the second copy became nonfunctional due to multiple deletions but Oryza brachyantha and Oryza australiensis still have two functional Rca genes. Detailed analysis of the promoter region of the two copies among various plant species showed insertion of several transposable elements harboring heat responsive elements in the heat inducible copy of the gene. The conserved RCA copy of wheat didn't have any transposable insertions whereas in that of maize has one heat shock element and sorghum had two. It would be interesting to study if the higher level of heat stress tolerance observed in sorghum and maize is associated with the differences observed for RCA. Key message This manuscript is reporting a grass family-specific tandem duplication event in RCA genes of cereals. The duplicated copies underwent neo-functionalization to evolve novel function to deal with heat stress. One copy of the tandem duplication maintained a high level of conservation whereas the second copy showed tremendous divergence to evolve species specific function of the gene. Specific function to respond to heat stress likely evolved via the insertion of various heat responsive elements carried by transposable elements.</p>","PeriodicalId":20064,"journal":{"name":"Plant Molecular Biology","volume":"115 1","pages":"10"},"PeriodicalIF":3.9,"publicationDate":"2024-12-21","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142872789","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}
Inorganic polyphosphate (polyP) is a linear polymer of phosphate that plays various roles in cells, including in phosphate and metal homeostasis. Homologs of the vacuolar transporter chaperone 4 (VTC4), catalyzing polyP synthesis in many eukaryotes, are absent in red algae, which are among the earliest divergent plant lineages. We identified homologs of polyphosphate kinase 1 (PPK1), a conserved polyP synthase in bacteria, in 42 eukaryotic genomes, including 31 species detected in this study and 12 species of red algae. Phylogenetic analysis suggested that most eukaryotic PPK1 homologs originated from horizontal gene transfer from a prokaryote to a plant before the divergence of red algae and Viridiplantae. In red algae, the homologs were fused to a nucleoside diphosphate-linked moiety X (Nudix) hydrolase of the diphosphoinositol polyphosphate phosphohydrolase (DIPP) family. We characterized the fusion protein CmPPK1 in the unicellular red alga Cyanidioschyzon merolae, which has been used in studies on basic features of eukaryotes. In the knockout strain ∆CmPPK1, polyP was undetectable, suggesting a primary role for CmPPK1 in polyP synthesis. In addition, ∆CmPPK1 showed altered metal balance. Mutations in the catalytically important residues of the Nudix hydrolase domain (NHD) either increased or decreased polyP contents. Both high and low polyP NHD mutants were susceptible to phosphate deprivation, indicating that adequate NHD function is necessary for normal phosphate starvation responses. The results reveal the unique features of PPK1 in red algae and promote further investigation of polyP metabolism and functions in red algae and eukaryotic evolution.
{"title":"A fusion protein of polyphosphate kinase 1 (PPK1) and a Nudix hydrolase is involved in inorganic polyphosphate accumulation in the unicellular red alga Cyanidioschyzon merolae.","authors":"Fumi Yagisawa, Takayuki Fujiwara, Shota Yamashita, Shunsuke Hirooka, Kei Tamashiro, Jin Izumi, Yu Kanesaki, Ryo Onuma, Osami Misumi, Soichi Nakamura, Hirofumi Yoshikawa, Haruko Kuroiwa, Tsuneyoshi Kuroiwa, Shin-Ya Miyagishima","doi":"10.1007/s11103-024-01539-5","DOIUrl":"10.1007/s11103-024-01539-5","url":null,"abstract":"<p><p>Inorganic polyphosphate (polyP) is a linear polymer of phosphate that plays various roles in cells, including in phosphate and metal homeostasis. Homologs of the vacuolar transporter chaperone 4 (VTC4), catalyzing polyP synthesis in many eukaryotes, are absent in red algae, which are among the earliest divergent plant lineages. We identified homologs of polyphosphate kinase 1 (PPK1), a conserved polyP synthase in bacteria, in 42 eukaryotic genomes, including 31 species detected in this study and 12 species of red algae. Phylogenetic analysis suggested that most eukaryotic PPK1 homologs originated from horizontal gene transfer from a prokaryote to a plant before the divergence of red algae and Viridiplantae. In red algae, the homologs were fused to a nucleoside diphosphate-linked moiety X (Nudix) hydrolase of the diphosphoinositol polyphosphate phosphohydrolase (DIPP) family. We characterized the fusion protein CmPPK1 in the unicellular red alga Cyanidioschyzon merolae, which has been used in studies on basic features of eukaryotes. In the knockout strain ∆CmPPK1, polyP was undetectable, suggesting a primary role for CmPPK1 in polyP synthesis. In addition, ∆CmPPK1 showed altered metal balance. Mutations in the catalytically important residues of the Nudix hydrolase domain (NHD) either increased or decreased polyP contents. Both high and low polyP NHD mutants were susceptible to phosphate deprivation, indicating that adequate NHD function is necessary for normal phosphate starvation responses. The results reveal the unique features of PPK1 in red algae and promote further investigation of polyP metabolism and functions in red algae and eukaryotic evolution.</p>","PeriodicalId":20064,"journal":{"name":"Plant Molecular Biology","volume":"115 1","pages":"9"},"PeriodicalIF":3.9,"publicationDate":"2024-12-19","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142855016","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}
We previously reported that in Arabidopsis, the phytochelatin-mediated metal-detoxification machinery is also essential for organomercurial phenylmercury (PheHg) tolerance. PheHg treatment causes severe root growth inhibition in cad1-3, an Arabidopsis phytochelatin-deficient mutant, frequently accompanied by abnormal root tip swelling. Here, we examine morphological and physiological characteristics of PheHg-induced abnormal root tip swelling in comparison to Hg(II) stress and demonstrate that auxin homeostasis disorder in the root is associated with the PheHg-induced root tip swelling. Both Hg(II) and PheHg treatments severely inhibited root growth in cad1-3 and simultaneously induced the disappearance of starch-containing plastid amyloplasts in columella cells. However, further confocal imaging of the root tip revealed distinct effects of Hg(II) and PheHg toxicity on root cell morphology. PheHg treatment suppressed most major genes involved in auxin homeostasis, whereas these expression levels were up-regulated after 24 h of Hg(II) treatment. PheHg-triggered suppression of auxin transporters PIN1, PIN2, and PIN3 as GFP-fusion proteins was observed in the root tip, accompanied by an auxin reporter DR5rev::GFP signal reduction. Supplementation of indole-3-acetic acid (IAA) drastically canceled the PheHg-induced root swelling, however, Hg(II) toxicity was not mitigated by IAA. The presented results show that the collapse of auxin homeostasis especially in root tips is a cause for the abnormal root tip swelling under PheHg stress conditions.
{"title":"Phenylmercury stress induces root tip swelling through auxin homeostasis disruption.","authors":"Shimpei Uraguchi, Masakazu Sato, Chihiro Hagai, Momoko Hirakawa, Kotomi Ogawa, Miyu Odagiri, Haruka Sato, Ayaka Ohmori, Yuka Ohshiro, Ryosuke Nakamura, Yasukazu Takanezawa, Masako Kiyono","doi":"10.1007/s11103-024-01538-6","DOIUrl":"10.1007/s11103-024-01538-6","url":null,"abstract":"<p><p>We previously reported that in Arabidopsis, the phytochelatin-mediated metal-detoxification machinery is also essential for organomercurial phenylmercury (PheHg) tolerance. PheHg treatment causes severe root growth inhibition in cad1-3, an Arabidopsis phytochelatin-deficient mutant, frequently accompanied by abnormal root tip swelling. Here, we examine morphological and physiological characteristics of PheHg-induced abnormal root tip swelling in comparison to Hg(II) stress and demonstrate that auxin homeostasis disorder in the root is associated with the PheHg-induced root tip swelling. Both Hg(II) and PheHg treatments severely inhibited root growth in cad1-3 and simultaneously induced the disappearance of starch-containing plastid amyloplasts in columella cells. However, further confocal imaging of the root tip revealed distinct effects of Hg(II) and PheHg toxicity on root cell morphology. PheHg treatment suppressed most major genes involved in auxin homeostasis, whereas these expression levels were up-regulated after 24 h of Hg(II) treatment. PheHg-triggered suppression of auxin transporters PIN1, PIN2, and PIN3 as GFP-fusion proteins was observed in the root tip, accompanied by an auxin reporter DR5rev::GFP signal reduction. Supplementation of indole-3-acetic acid (IAA) drastically canceled the PheHg-induced root swelling, however, Hg(II) toxicity was not mitigated by IAA. The presented results show that the collapse of auxin homeostasis especially in root tips is a cause for the abnormal root tip swelling under PheHg stress conditions.</p>","PeriodicalId":20064,"journal":{"name":"Plant Molecular Biology","volume":"115 1","pages":"8"},"PeriodicalIF":3.9,"publicationDate":"2024-12-18","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11655593/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142855019","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}
Pub Date : 2024-12-17DOI: 10.1007/s11103-024-01532-y
Adrián González Ortega-Villaizán, Eoghan King, Manish K Patel, Estefanía Rodríguez-Dobreva, Marcia González-Teuber, Patricio Ramos, Jesús Vicente-Carbajosa, Begoña Benito, Stephan Pollmann
Global climate change exacerbates abiotic stresses, as drought, heat, and salt stresses are anticipated to increase significantly in the coming years. Plants coexist with a diverse range of microorganisms. Multiple inter-organismic relationships are known to confer benefits to plants, including growth promotion and enhanced tolerance to abiotic stresses. In this study, we investigated the mutualistic interactions between three fungal endophytes originally isolated from distinct arid environments and an agronomically relevant crop, Solanum lycopersicum. We demonstrated a significant increase in shoot biomass under drought conditions in co-cultivation with Penicillium chrysogenum isolated from Antarctica, Penicillium minioluteum isolated from the Atacama Desert, Chile, and Serendipita indica isolated from the Thar Desert, India. To elucidate plant gene modules commonly induced by the different endophytes that could explain the observed drought tolerance effect in tomato, a comprehensive transcriptomics analysis was conducted. This analysis led to the identification of a shared gene module in the fungus-infected tomato plants. Within this module, gene network analysis enabled us to identify genes related to abscisic acid (ABA) signaling, ABA transport, auxin signaling, ion homeostasis, proline biosynthesis, and jasmonic acid signaling, providing insights into the molecular basis of drought tolerance commonly mediated by fungal endophytes. Our findings highlight a conserved response in the mutualistic interactions between endophytic fungi isolated from unrelated environments and tomato roots, resulting in improved shoot biomass production under drought stress.
{"title":"Identification of a drought stress response module in tomato plants commonly induced by fungal endophytes that confer increased drought tolerance.","authors":"Adrián González Ortega-Villaizán, Eoghan King, Manish K Patel, Estefanía Rodríguez-Dobreva, Marcia González-Teuber, Patricio Ramos, Jesús Vicente-Carbajosa, Begoña Benito, Stephan Pollmann","doi":"10.1007/s11103-024-01532-y","DOIUrl":"10.1007/s11103-024-01532-y","url":null,"abstract":"<p><p>Global climate change exacerbates abiotic stresses, as drought, heat, and salt stresses are anticipated to increase significantly in the coming years. Plants coexist with a diverse range of microorganisms. Multiple inter-organismic relationships are known to confer benefits to plants, including growth promotion and enhanced tolerance to abiotic stresses. In this study, we investigated the mutualistic interactions between three fungal endophytes originally isolated from distinct arid environments and an agronomically relevant crop, Solanum lycopersicum. We demonstrated a significant increase in shoot biomass under drought conditions in co-cultivation with Penicillium chrysogenum isolated from Antarctica, Penicillium minioluteum isolated from the Atacama Desert, Chile, and Serendipita indica isolated from the Thar Desert, India. To elucidate plant gene modules commonly induced by the different endophytes that could explain the observed drought tolerance effect in tomato, a comprehensive transcriptomics analysis was conducted. This analysis led to the identification of a shared gene module in the fungus-infected tomato plants. Within this module, gene network analysis enabled us to identify genes related to abscisic acid (ABA) signaling, ABA transport, auxin signaling, ion homeostasis, proline biosynthesis, and jasmonic acid signaling, providing insights into the molecular basis of drought tolerance commonly mediated by fungal endophytes. Our findings highlight a conserved response in the mutualistic interactions between endophytic fungi isolated from unrelated environments and tomato roots, resulting in improved shoot biomass production under drought stress.</p>","PeriodicalId":20064,"journal":{"name":"Plant Molecular Biology","volume":"115 1","pages":"7"},"PeriodicalIF":3.9,"publicationDate":"2024-12-17","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11652604/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142847250","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}
Pub Date : 2024-12-16DOI: 10.1007/s11103-024-01540-y
Sebastian Buitrago, Xinsun Yang, Lianjun Wang, Rui Pan, Wenying Zhang
Anthocyanin regulation can be fruitfully explored from a diverse perspective by studying distantly related model organisms. Land plants pioneers faced a huge evolutionary leap, involving substantial physiological and genetic changes. Anthocyanins have evolved alongside these changes, becoming versatile compounds capable of mitigating terrestrial challenges such as drought, salinity, extreme temperatures and high radiation. With the accessibility of whole-genome sequences from ancient plant lineages, deeper insights into the evolution of key metabolic pathways like phenylpropanoids have emerged. Despite understanding the function of anthocyanins under stress, gaps remain in uncovering the precise metabolic and regulatory mechanisms driving their overproduction under stressful conditions. For example, the regulatory effect of reactive oxygen species (ROS) on well-known transcription factors like MYBs is not fully elucidated. This manuscript presents an evolutionary analysis of the anthocyanin biosynthetic pathway to elucidate key genes. CINNAMATE 4-HYDROXYLASE (C4H) and CHALCONE ISOMERASE (CHI2) received particular attention. C4H exposes remarkable differences between aquatic and land plants, while CHI2 demonstrates substantial variation in gene copy number and sequence similarity across species. The role of transcription factors, such as MYB, and the involvement of ROS in the regulation of anthocyanin biosynthesis are discussed. Complementary gene expression analyses under abiotic stress in Arabidopsis thaliana, Selaginella moellendorffii, and Marchantia polymorpha reveal intriguing gene-stress relationships. This study highlights evolutionary trends and the regulatory complexity of anthocyanin production under abiotic stress, providing insights and opening avenues for future research.
{"title":"Evolutionary analysis of anthocyanin biosynthetic genes: insights into abiotic stress adaptation.","authors":"Sebastian Buitrago, Xinsun Yang, Lianjun Wang, Rui Pan, Wenying Zhang","doi":"10.1007/s11103-024-01540-y","DOIUrl":"10.1007/s11103-024-01540-y","url":null,"abstract":"<p><p>Anthocyanin regulation can be fruitfully explored from a diverse perspective by studying distantly related model organisms. Land plants pioneers faced a huge evolutionary leap, involving substantial physiological and genetic changes. Anthocyanins have evolved alongside these changes, becoming versatile compounds capable of mitigating terrestrial challenges such as drought, salinity, extreme temperatures and high radiation. With the accessibility of whole-genome sequences from ancient plant lineages, deeper insights into the evolution of key metabolic pathways like phenylpropanoids have emerged. Despite understanding the function of anthocyanins under stress, gaps remain in uncovering the precise metabolic and regulatory mechanisms driving their overproduction under stressful conditions. For example, the regulatory effect of reactive oxygen species (ROS) on well-known transcription factors like MYBs is not fully elucidated. This manuscript presents an evolutionary analysis of the anthocyanin biosynthetic pathway to elucidate key genes. CINNAMATE 4-HYDROXYLASE (C4H) and CHALCONE ISOMERASE (CHI2) received particular attention. C4H exposes remarkable differences between aquatic and land plants, while CHI2 demonstrates substantial variation in gene copy number and sequence similarity across species. The role of transcription factors, such as MYB, and the involvement of ROS in the regulation of anthocyanin biosynthesis are discussed. Complementary gene expression analyses under abiotic stress in Arabidopsis thaliana, Selaginella moellendorffii, and Marchantia polymorpha reveal intriguing gene-stress relationships. This study highlights evolutionary trends and the regulatory complexity of anthocyanin production under abiotic stress, providing insights and opening avenues for future research.</p>","PeriodicalId":20064,"journal":{"name":"Plant Molecular Biology","volume":"115 1","pages":"6"},"PeriodicalIF":3.9,"publicationDate":"2024-12-16","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142829745","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}
Pub Date : 2024-12-13DOI: 10.1007/s11103-024-01536-8
Jing Cao, Ayixianmuguli Maitirouzi, Yudan Feng, Hua Zhang, Youqiang Heng, Jinbo Zhang, Yan Wang
Pathogenesis-related proteins (PR), whose expressions are induced by biotic and abiotic stress, play important roles in plant defense. Previous research identified the salt-induced HcPR10 gene in the halophyte Halostachys caspica as a regulator of plant growth and development through interactions with cytokinin. However, the mechanisms by which HcPR10 mediates resistance to abiotic stress remain poorly understood. In this study, we found that the heterologous expression of HcPR10 significantly enhanced salt and drought tolerance in Arabidopsis, likely by increasing the activity of antioxidant enzyme systems, allowing for effective scavenging of reactive oxygen species (ROS) and thus protecting plant cells from oxidative damage. Additionally, the overexpression of HcPR10 also activated the expression of stress-related genes in Arabidopsis. Furthermore, using yeast two-hybrid technology, five proteins (HcLTPG6, HcGPX6, HcUGT73B3, HcLHCB2.2, and HcMSA1) were identified as potential interacting partners for HcPR10, which could positively regulate the salt stress response mediated by HcPR10. Our findings lay the foundation for a better understanding of the molecular mechanisms of HcPR10 in response to abiotic stress and reveal additional candidate genes for improving crop salt tolerance through genetic engineering.
{"title":"Heterologous expression of Halostachys caspica pathogenesis-related protein 10 increases salt and drought resistance in transgenic Arabidopsis thaliana.","authors":"Jing Cao, Ayixianmuguli Maitirouzi, Yudan Feng, Hua Zhang, Youqiang Heng, Jinbo Zhang, Yan Wang","doi":"10.1007/s11103-024-01536-8","DOIUrl":"10.1007/s11103-024-01536-8","url":null,"abstract":"<p><p>Pathogenesis-related proteins (PR), whose expressions are induced by biotic and abiotic stress, play important roles in plant defense. Previous research identified the salt-induced HcPR10 gene in the halophyte Halostachys caspica as a regulator of plant growth and development through interactions with cytokinin. However, the mechanisms by which HcPR10 mediates resistance to abiotic stress remain poorly understood. In this study, we found that the heterologous expression of HcPR10 significantly enhanced salt and drought tolerance in Arabidopsis, likely by increasing the activity of antioxidant enzyme systems, allowing for effective scavenging of reactive oxygen species (ROS) and thus protecting plant cells from oxidative damage. Additionally, the overexpression of HcPR10 also activated the expression of stress-related genes in Arabidopsis. Furthermore, using yeast two-hybrid technology, five proteins (HcLTPG6, HcGPX6, HcUGT73B3, HcLHCB2.2, and HcMSA1) were identified as potential interacting partners for HcPR10, which could positively regulate the salt stress response mediated by HcPR10. Our findings lay the foundation for a better understanding of the molecular mechanisms of HcPR10 in response to abiotic stress and reveal additional candidate genes for improving crop salt tolerance through genetic engineering.</p>","PeriodicalId":20064,"journal":{"name":"Plant Molecular Biology","volume":"115 1","pages":"5"},"PeriodicalIF":3.9,"publicationDate":"2024-12-13","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142818949","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}
Pub Date : 2024-12-12DOI: 10.1007/s11103-024-01521-1
Rosa Irma Obando-González, Luis Enrique Martínez-Hernández, Leandro Alberto Núñez-Muñoz, Berenice Calderón-Pérez, Roberto Ruiz-Medrano, José Abrahán Ramírez-Pool, Beatriz Xoconostle-Cázares
Plant breeding plays a pivotal role in the development of improved tomato cultivars, addressing various challenges faced by this crop worldwide. Tomato crop yield is affected by biotic and abiotic stress, including diverse pathogens and pests, extreme temperatures, drought, and soil salinity, thus affecting fruit quality, and overall crop productivity. Through strategic plant breeding approaches, it is possible to increase the genetic diversity of tomato cultivars, leading to the development of varieties with increased resistance to prevalent diseases and pests, improved tolerance to environmental stress, and enhanced adaptability to changing agroclimatic conditions. The induction of genetic variability using antimitotic agents, such as colchicine, has been widely employed in plant breeding precisely to this end. In this study, we analyzed the transcriptome of colchicine-treated tomato plants exhibiting larger size, characterized by larger leaves, while seedlings of the T2 generation harbored three cotyledons. A total of 382 differentially expressed genes encoding proteins associated with anatomical structure development, hormone synthesis and transport, flavonoid biosynthesis, and responses to various stimuli, stresses, and defense mechanisms were identified. Gene enrichment analysis suggests a role for auxin and flavonoid biosynthesis in cotyledon formation. Furthermore, single-nucleotide polymorphisms were mapped in colchicine-treated plants and determined which corresponded to differentially- expressed genes. Interestingly, most were associated to only a few genes in a similar location. This study provides significant insights into the genes and metabolic pathways affected in colchicine-treated tomatoes that exhibit improved agronomic traits, such as plant vigor and improved photosynthesis rate.
{"title":"Plant growth Enhancement in Colchicine-Treated Tomato Seeds without Polyploidy Induction.","authors":"Rosa Irma Obando-González, Luis Enrique Martínez-Hernández, Leandro Alberto Núñez-Muñoz, Berenice Calderón-Pérez, Roberto Ruiz-Medrano, José Abrahán Ramírez-Pool, Beatriz Xoconostle-Cázares","doi":"10.1007/s11103-024-01521-1","DOIUrl":"10.1007/s11103-024-01521-1","url":null,"abstract":"<p><p>Plant breeding plays a pivotal role in the development of improved tomato cultivars, addressing various challenges faced by this crop worldwide. Tomato crop yield is affected by biotic and abiotic stress, including diverse pathogens and pests, extreme temperatures, drought, and soil salinity, thus affecting fruit quality, and overall crop productivity. Through strategic plant breeding approaches, it is possible to increase the genetic diversity of tomato cultivars, leading to the development of varieties with increased resistance to prevalent diseases and pests, improved tolerance to environmental stress, and enhanced adaptability to changing agroclimatic conditions. The induction of genetic variability using antimitotic agents, such as colchicine, has been widely employed in plant breeding precisely to this end. In this study, we analyzed the transcriptome of colchicine-treated tomato plants exhibiting larger size, characterized by larger leaves, while seedlings of the T2 generation harbored three cotyledons. A total of 382 differentially expressed genes encoding proteins associated with anatomical structure development, hormone synthesis and transport, flavonoid biosynthesis, and responses to various stimuli, stresses, and defense mechanisms were identified. Gene enrichment analysis suggests a role for auxin and flavonoid biosynthesis in cotyledon formation. Furthermore, single-nucleotide polymorphisms were mapped in colchicine-treated plants and determined which corresponded to differentially- expressed genes. Interestingly, most were associated to only a few genes in a similar location. This study provides significant insights into the genes and metabolic pathways affected in colchicine-treated tomatoes that exhibit improved agronomic traits, such as plant vigor and improved photosynthesis rate.</p>","PeriodicalId":20064,"journal":{"name":"Plant Molecular Biology","volume":"115 1","pages":"3"},"PeriodicalIF":3.9,"publicationDate":"2024-12-12","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11638462/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142818950","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}