{"title":"Construction of a non-coding RNA-mediated metabolic regulatory network to explore metabolic variation in tomato breeding","authors":"Penghui Liu, Chao Wang, Zhonghui Zhang, Ziyue Xu, Xumin Ou, Shixuan Li, Jianing Zhang, Yingchen Hao, Peng Cao, Cang Zhao, Yuanyuan Tang, Meng Deng, Jun Yang, Shouchuang Wang","doi":"10.1093/plphys/kiaf223","DOIUrl":"https://doi.org/10.1093/plphys/kiaf223","url":null,"abstract":"Tomato (Solanum lycopersicum), an economically important crop rich in secondary metabolites, serves as a model organism for studying secondary metabolism. However, research into how non-coding RNAs (ncRNAs) regulate metabolite accumulation in tomato is limited. Here, we identified and characterized 418 miRNAs in three tomato subgroups: Solanum pimpinellifolium (SP), Solanum lycopersicum var. cerasiforme (SLC), and Solanum lycopersicum var. lycopersicum (SLL). Notably, the Solanum pimpinellifolium genome exhibited the highest number of missing miRNAs, with targets linked to sugar metabolism. Next, we identified 133 miRNAs that were up-regulated during domestication; their target genes were associated with plant development and morphogenesis. Additionally, 2,938 long non-coding RNAs (lncRNAs) were identified and characterized, with intergenic lncRNAs being the most abundant type (70.2% of all lncRNAs). A total of 280 metabolites were identified from multiple tissues (flavonoids, steroidal glycoalkaloids, etc), and the steroidal glycoalkaloid content of all tissues was associated with domestication status. Finally, we constructed a ncRNA-mediated metabolic regulatory network for tomato, which included 369 lncRNA-miRNA pairs, 5,659 miRNA-mRNA pairs, and 136,599 mRNA-metabolite pairs. We found that miR172 isoforms target a UDP-glycosyltransferase (SlUGT71T212), which is involved in the glycosylation of flavonoids, and we validated the role of the miR172a-SlUGT71T212 module in the formation of naringenin-O-glycoside. Our study provides a comprehensive and valuable dataset of ncRNAs and metabolites in tomato. The ncRNA-mediated metabolic regulatory network is a useful theoretical resource for elucidating metabolic variation and its regulation during tomato breeding.","PeriodicalId":20101,"journal":{"name":"Plant Physiology","volume":"164 1","pages":""},"PeriodicalIF":7.4,"publicationDate":"2025-06-05","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"144228630","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}
Plant PhysiologyPub Date : 2025-06-03DOI: 10.1093/plphys/kiaf216
Liping Wang, You Wang, Regina Feil, Gregory J MacNeill, John E Lunn, Ian J Tetlow, Michael J Emes
{"title":"Plastidial starch phosphorylase regulates maltodextrin turnover during starch granule initiation in Arabidopsis leaves","authors":"Liping Wang, You Wang, Regina Feil, Gregory J MacNeill, John E Lunn, Ian J Tetlow, Michael J Emes","doi":"10.1093/plphys/kiaf216","DOIUrl":"https://doi.org/10.1093/plphys/kiaf216","url":null,"abstract":"PLASTIDIAL STARCH PHOSPHORYLASE 1 (PHS1) is considered integral to starch synthesis, yet its role in transient starch synthesis in photosynthetic tissues remains unclear, as mutation of PHS1 in Arabidopsis (Arabidopsis thaliana) does not affect the metabolic profile of leaves. PHS1 activity is elevated in the starch branching enzyme sbe2.1 sbe2.2 double mutant, which lacks starch granules but retains intact genes encoding granule initiation proteins, making it an ideal plant material for exploring PHS1 function. We generated a triple mutant, sbe2.1 sbe2.2 phs1-1, which showed additional accumulation of soluble maltodextrins, a loss of insoluble linear α-glucans in the leaves, and substantially retarded plant growth, compared to the sbe2.1 sbe2.2 double mutant. STARCH SYNTHASE 3 (SS3) and SS4 activities increased in the sbe2.1 sbe2.2 phs1-1 triple mutant relative to the sbe2.1 sbe2.2 double mutant. Additional loss of SS4 in the sbe2.1 sbe2.2 phs1-1 background partially reversed phenotypes observed in the triple mutant: maltodextrin content decreased, insoluble α-glucans reappeared, and plant growth improved. Principal component analysis revealed that the metabolite profile of the sbe2.1 sbe2.2 ss4 and sbe2.1 sbe2.2 phs1-1 ss4 mutants, particularly the levels of organic acids from the tricarboxylic acid cycle, more closely resembled that of the wild type than that of sbe2.1 sbe2.2 and sbe2.1 sbe2.2 phs1-1. These findings suggest that PHS1 plays a critical role in maltodextrin turnover and carbon regulation in chloroplasts, maintaining a coordinated balance of synthetic and degradative activities. We propose that PHS1 functions as a metabolic buffer, with its role becoming more crucial when starch synthesis pathways are disrupted.","PeriodicalId":20101,"journal":{"name":"Plant Physiology","volume":"329 1","pages":""},"PeriodicalIF":7.4,"publicationDate":"2025-06-03","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"144210843","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}
Plant PhysiologyPub Date : 2025-06-03DOI: 10.1093/plphys/kiaf219
Yanliang Guo, Jiayue Li, Lingling Liu, Jiahe Liu, Chao Li, Li Yuan, Chunhua Wei, Xian Zhang, Hao Li
{"title":"The Ca2+ channels CNGC2 and CNGC20 mediate methyl jasmonate-induced calcium signaling and cold tolerance","authors":"Yanliang Guo, Jiayue Li, Lingling Liu, Jiahe Liu, Chao Li, Li Yuan, Chunhua Wei, Xian Zhang, Hao Li","doi":"10.1093/plphys/kiaf219","DOIUrl":"https://doi.org/10.1093/plphys/kiaf219","url":null,"abstract":"The phytohormone methyl jasmonate (MeJA) enhances plant cold stress tolerance, but the underlying mechanisms remain elusive. Here, we discovered that MeJA induces a transient Ca2+ influx and elevated cytoplasmic free Ca2+ ([Ca2+]cyt) levels during the watermelon (Citrullus lanatus) response to cold stress. Conversely, silencing jasmonic acid carboxyl methyltransferase (ClJMT), encoding an enzyme that methylates JA to MeJA, led to contrasting effects compared to MeJA application. Upon cold exposure, MeJA rapidly and continuously upregulated two Ca2+-permeable channel genes, namely cyclic nucleotide-gated ion channel (ClCNGC) 2 and ClCNGC20. Silencing ClCNGC2 or ClCNGC20 attenuated MeJA-induced Ca2+ influx, [Ca2+]cyt accumulation, C-REPEAT BINDING FACTOR (CBF) pathway activation, and watermelon cold tolerance. Accordingly, ClCNGC2 or ClCNGC20 overexpression increased Ca2+ influx, [Ca2+]cyt levels, and expression of the CBF regulon, and improved freezing tolerance in transgenic Arabidopsis thaliana plants. Multiple assays showed that ClCNGC2 and ClCNGC20 do not directly interact. Interestingly, silencing ClCNGC2 or ClCNGC20 abolished MeJA-induced upregulation of ClCNGC20 or ClCNGC2, respectively, in watermelon response to cold, demonstrating their reciprocal activation at the transcriptional level. Collectively, these findings suggest a mutual dependence between ClCNGC2 and ClCNGC20 in mediating MeJA-induced Ca2+ influx followed by [Ca2+]cyt elevation, subsequently activating the CBF pathway and enhancing cold tolerance in plants. This study provides insights into the molecular mechanisms underlying MeJA-mediated plant cold tolerance, holding potential for the breeding or engineering of cold-resistant cucurbit varieties.","PeriodicalId":20101,"journal":{"name":"Plant Physiology","volume":"41 1","pages":""},"PeriodicalIF":7.4,"publicationDate":"2025-06-03","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"144210858","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}
Plant PhysiologyPub Date : 2025-06-03DOI: 10.1093/plphys/kiaf215
Ian W McCahill, Logayn T Abushal, Bahman Khahani, Cassandra F Probert, Eleah L Flockhart, Greg A Gregory, Edward Z Li, Yu Zhang, Leo A Baumgart, Ronan C O'Malley, Samuel P Hazen
{"title":"Shoring up the base: the development and regulation of cortical sclerenchyma in grass nodal roots","authors":"Ian W McCahill, Logayn T Abushal, Bahman Khahani, Cassandra F Probert, Eleah L Flockhart, Greg A Gregory, Edward Z Li, Yu Zhang, Leo A Baumgart, Ronan C O'Malley, Samuel P Hazen","doi":"10.1093/plphys/kiaf215","DOIUrl":"https://doi.org/10.1093/plphys/kiaf215","url":null,"abstract":"Plants depend on the combined action of a shoot-root-soil system to maintain their anchorage to the soil. Mechanical failure of any component of this system results in lodging, a permanent and irreversible inability to maintain vertical orientation. Models of anchorage in grass crops identify the compressive strength of roots near the soil surface as the key determinant of resistance to lodging. Indeed, studies of disparate grasses report a ring of thickened sclerenchyma cells surrounding the root cortex, present only at the base of nodal roots. Here, in the investigation of the development and regulation of this agronomically important trait, we used the model species Brachypodium distachyon and show that development of these cells is uncoupled from the maturation of other secondary cell wall-fortified cells and that cortical sclerenchyma wall thickening is stimulated by mechanical forces transduced from the shoot to the root. We also show that exogenous application of gibberellic acid stimulates thickening of lignified cell types in the root, including cortical sclerenchyma, but is not sufficient to establish sclerenchyma identity in cortex cells. Leveraging the ability to manipulate cortex development via mechanical stimulus, we show that cortical sclerenchyma development alters root mechanical properties and improves resistance to lodging. We describe transcriptome changes associated with cortical sclerenchyma development under both ambient and mechanically stimulated conditions and identify SECONDARY WALL NAC7 as a putative regulator of mechanically responsive cortex cell wall development at the root base. Overall, our findings show that grasses use a coordinated system involving mechanoperception, phytohormone signaling, and transcriptional regulation to modulate investment in cortical sclerenchyma, proactively reinforcing anchorage in response to mechanical challenges.","PeriodicalId":20101,"journal":{"name":"Plant Physiology","volume":"20 1","pages":""},"PeriodicalIF":7.4,"publicationDate":"2025-06-03","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"144210842","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}
Plant PhysiologyPub Date : 2025-06-03DOI: 10.1093/plphys/kiaf218
Ping-Li Liu, Zhao-Yang Jing, Ren-Gang Zhang, Ye Chen, Zhixin Zhu, Xi Zhang, Chen-Kun Jiang, Ruili Li, Jian-Bo Xie, Shihui Niu, Jinfeng Zhang, Lisheng Kong, Jian Zhao, Yongpeng Ma, Viktoria V Zeisler-Diehl, Lukas Schreiber, Ichirou Karahara, Jian-Feng Mao, Yuannian Jiao, Song Ge, Jinxing Lin
{"title":"Genomic insights into the evolution of Chinese sweetgum and its autumn leaf coloration","authors":"Ping-Li Liu, Zhao-Yang Jing, Ren-Gang Zhang, Ye Chen, Zhixin Zhu, Xi Zhang, Chen-Kun Jiang, Ruili Li, Jian-Bo Xie, Shihui Niu, Jinfeng Zhang, Lisheng Kong, Jian Zhao, Yongpeng Ma, Viktoria V Zeisler-Diehl, Lukas Schreiber, Ichirou Karahara, Jian-Feng Mao, Yuannian Jiao, Song Ge, Jinxing Lin","doi":"10.1093/plphys/kiaf218","DOIUrl":"https://doi.org/10.1093/plphys/kiaf218","url":null,"abstract":"Chinese sweetgum (Liquidambar formosana) is valued as a source of resin and timber and is an important ornamental tree due to its showy fall foliage. Here, we report the chromosome-level assembly of the Chinese sweetgum genome. Phylogenomic analyses showed the basal phylogenetic position of Chinese sweetgum in core eudicots. Comparative genomic analyses revealed that the well-known gamma event in the common ancestors of core eudicots is evident in the Chinese sweetgum genome, and ancestral triplicated blocks resulting from that event are more intact in Chinese sweetgum than in grapevine (Vitis vinifera). Because of its conserved genome structure, very slow rate of evolution, and basal phylogenetic position, the Chinese sweetgum genome is a good reference for comparative genome studies. Further, we reconstructed the entire metabolic pathway for anthocyanins and potential regulatory networks of autumn leaf coloration of this species via metabolomics and transcriptomics. The transcription factors LfMYB69, basic helix–loop–helix (LfbHLH4), and WD40-repeat (LfWDR1) may collectively regulate the transcription of anthocyanin biosynthetic genes. The regulation of chalcone synthase genes (LfCHS1-3) and dihydroflavonol 4-reductase genes (LfDFR1-2) by the LfMYB69-LfbHLH4-LfWDR1 complex was confirmed by luciferase assays. Epigenomic analyses revealed that five structural genes, including LfCHS1, and two regulatory LfMYBs are epigenetically regulated. This study expands our understanding of autumn leaf coloration and provides valuable genomic resources for comparative biology, breeding, and biotechnology.","PeriodicalId":20101,"journal":{"name":"Plant Physiology","volume":"13 1","pages":""},"PeriodicalIF":7.4,"publicationDate":"2025-06-03","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"144210873","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
{"title":"The transcription factor Dof32 coordinates salvianolic acid biosynthesis and drought tolerance in Salvia miltiorrhiza","authors":"Bingbing Lv, Qiaoqiao Feng, Gaige Shao, Anqi Zuo, Xuejiao Yan, Jingying Liu, Juane Dong, Pengda Ma","doi":"10.1093/plphys/kiaf221","DOIUrl":"https://doi.org/10.1093/plphys/kiaf221","url":null,"abstract":"Drought severely impacts plant growth, yet moderate drought stress can stimulate the biosynthesis of active compounds in medicinal plants. However, the molecular regulators and mechanisms linking drought resistance with the accumulation of active compounds remain poorly understood. In this study, we identified the Dof transcription factor SmDof32 as a key regulator of both salvianolic acid biosynthesis and the drought response in Danshen (Salvia miltiorrhiza). Overexpression of SmDof32 enhanced both the accumulation of medicinal compounds and drought resistance, whereas SmDof32 RNA interference resulted in less accumulation of salvianolic acids and diminished drought tolerance. DNA-affinity purification sequencing (DAP-seq) combined with RNA-sequencing (RNA-seq) analysis revealed that SmDof32 directly promotes the expression of lipoxygenase (SmLOX8) and rosmarinic acid synthase (SmRAS1), thereby increasing the biosynthesis of jasmonic acid (JA) and salvianolic acids. Further analysis of SmLOX8 overexpression and RNAi lines confirmed that SmLOX8 promotes JA biosynthesis, enhances drought tolerance, and increases salvianolic acid biosynthesis. Moreover, inhibition of JA biosynthesis significantly reduced the positive effects of SmDof32 on salvianolic acid accumulation and drought tolerance. Collectively, these findings suggest that the SmDof32-SmLOX8/SmRAS1 module plays a crucial role in the drought response and accumulation of salvianolic acids, providing genetic targets for breeding S. miltiorrhiza with enhanced medicinal compound content and drought resilience.","PeriodicalId":20101,"journal":{"name":"Plant Physiology","volume":"54 1","pages":""},"PeriodicalIF":7.4,"publicationDate":"2025-06-03","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"144210844","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}
Plant PhysiologyPub Date : 2025-05-30DOI: 10.1093/plphys/kiaf251
Thomas Depaepe
{"title":"Partners in light: Vitamin E and the price of being green.","authors":"Thomas Depaepe","doi":"10.1093/plphys/kiaf251","DOIUrl":"10.1093/plphys/kiaf251","url":null,"abstract":"","PeriodicalId":20101,"journal":{"name":"Plant Physiology","volume":" ","pages":""},"PeriodicalIF":6.5,"publicationDate":"2025-05-30","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC12199778/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"144286115","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Plant PhysiologyPub Date : 2025-05-30DOI: 10.1093/plphys/kiaf207
Xianjun Zhang, Rin Taniguchi, Shen Ye, Yutaka Shibata
{"title":"Revealing the diversity of in vivo photosystem I light-harvesting antennae.","authors":"Xianjun Zhang, Rin Taniguchi, Shen Ye, Yutaka Shibata","doi":"10.1093/plphys/kiaf207","DOIUrl":"https://doi.org/10.1093/plphys/kiaf207","url":null,"abstract":"<p><p>The photosynthetic reaction is driven by the 2 light-excited pigment-protein supercomplexes: photosystem II (PSII) and photosystem I (PSI). Due to the low excitation probability of chlorophylls (Chls), the efficient excitation of the 2 PSs relies on the exquisite organization of their light-harvesting antenna under environmental fluctuations. However, since the antenna-protein composition within cells remains elusive, the in vivo events arising from antenna variations cannot be accurately explored. Here, we implemented the single-pixel excitation-emission spectroscopy of Chlamydomonas reinhardtii cells under 80 K using a cryogenic optical microscope. The antenna variations of in vivo PSI can be exclusively evaluated via this low-temperature spectro-imaging method. The simultaneous acquisition of 2 types of fluorescence spectra enables the analysis of the intracellular association between the PSII/PSI intensity ratio and the Chl-b/a intensity ratio. We found that the Chl-b/a intensity ratio hardly correlated with the PSII/PSI intensity ratio, suggesting that the in vivo PSII/PSI fluorescence intensity ratio reflects the relative PSII/PSI stoichiometry rather than their antenna sizes. More importantly, the analysis of the PSI antenna-related Chl-b contribution within cells reveals a mega-antenna system that has much larger antenna sizes than those of the PSI supercomplexes whose structures have been resolved so far. Such PSI megacomplexes tended to be enriched in the region surrounding the pyrenoids. We anticipate the present investigation to be a starting point for directly estimating the arrangements of antenna systems of photosystems at the single-cell scale, which is necessary for a deeper understanding of dynamic in vivo events related to the photosynthetic light-harvesting process.</p>","PeriodicalId":20101,"journal":{"name":"Plant Physiology","volume":"198 2","pages":""},"PeriodicalIF":6.5,"publicationDate":"2025-05-30","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"144317643","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}