Mamoona Khan, Nithya Nagarajan, Kathrin Schneewolf, Caroline Marcon, Danning Wang, Frank Hochholdinger, Peng Yu, Armin Djamei
Summary Biotrophic plant–pathogens secrete effector molecules to redirect and exploit endogenous signaling and developmental pathways in their favor. The biotrophic fungus Ustilago maydis causes galls on all aerial parts of maize. However, the responsible gall‐inducing effectors and corresponding plant signaling pathway(s) remain largely unknown. Using molecular and genetic approaches, and transcriptomic comparisons in maize, we identify downstream targets and developmental consequences of the plant TOPLESS (TPL)‐interacting protein (Tip) effectors in gall formation. We demonstrate that Tip4 derepress AtARF7/AtARF19 branch of auxin signaling, leading to the formation of pluripotent calli without the external addition of phytohormones. Comparative transcriptomics in maize further reveals a significant overlap of genes upregulated during U. maydis ‐triggered leaf gall formation and the developmental initiation of lateral roots (LRs). Additionally, we show that this process involves the transcriptional upregulation of downstream LATERAL ORGAN BOUNDARIES DOMAIN (LBD) transcription factors. Homozygous mutations in two LBD genes ( ra2 , rtcs ) resulted in significantly reduced gall formation in maize. Taken together, our results suggest that U. maydis hijacks the LR initiation pathway to trigger gall formation in maize shoots, revealing key effectors and host pathways exploited by biotrophic pathogens.
{"title":"Pathogenic fungus Ustilago maydis exploits the lateral root regulators to induce pluripotency in maize shoots","authors":"Mamoona Khan, Nithya Nagarajan, Kathrin Schneewolf, Caroline Marcon, Danning Wang, Frank Hochholdinger, Peng Yu, Armin Djamei","doi":"10.1111/nph.70843","DOIUrl":"https://doi.org/10.1111/nph.70843","url":null,"abstract":"Summary <jats:list list-type=\"bullet\"> <jats:list-item> Biotrophic plant–pathogens secrete effector molecules to redirect and exploit endogenous signaling and developmental pathways in their favor. The biotrophic fungus <jats:italic>Ustilago maydis</jats:italic> causes galls on all aerial parts of maize. However, the responsible gall‐inducing effectors and corresponding plant signaling pathway(s) remain largely unknown. </jats:list-item> <jats:list-item> Using molecular and genetic approaches, and transcriptomic comparisons in maize, we identify downstream targets and developmental consequences of the plant TOPLESS (TPL)‐interacting protein (Tip) effectors in gall formation. </jats:list-item> <jats:list-item> We demonstrate that Tip4 derepress <jats:italic>AtARF7/AtARF19</jats:italic> branch of auxin signaling, leading to the formation of pluripotent calli without the external addition of phytohormones. Comparative transcriptomics in maize further reveals a significant overlap of genes upregulated during <jats:italic>U. maydis</jats:italic> ‐triggered leaf gall formation and the developmental initiation of lateral roots (LRs). Additionally, we show that this process involves the transcriptional upregulation of downstream LATERAL ORGAN BOUNDARIES DOMAIN (LBD) transcription factors. Homozygous mutations in two LBD genes ( <jats:italic>ra2</jats:italic> , <jats:italic>rtcs</jats:italic> ) resulted in significantly reduced gall formation in maize. </jats:list-item> <jats:list-item> Taken together, our results suggest that <jats:italic>U. maydis</jats:italic> hijacks the LR initiation pathway to trigger gall formation in maize shoots, revealing key effectors and host pathways exploited by biotrophic pathogens. </jats:list-item> </jats:list>","PeriodicalId":214,"journal":{"name":"New Phytologist","volume":"9 1","pages":""},"PeriodicalIF":9.4,"publicationDate":"2025-12-27","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"145836225","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}
Summary RNA end maturation and stabilization are crucial for plant organellar gene expression, yet the mechanisms remain elusive, partially due to the lack of efficient RNA end mapping methods. We developed a high‐throughput transcript end mapping tool (Hiten) by integrating in vitro RNA circularization, next‐generation sequencing, and circRNA identification algorithm MeCi. Using Hiten, we systematically mapped 5′ and 3′ ends of organellar mRNAs and noncoding RNAs (ncRNAs) and characterized organellar polyadenosine tails in maize ( Zea mays ). Combining RNA 5′‐polyphosphatase treatment with Hiten demonstrates that transcription initiation plays a major role in 5′‐end formation of mRNAs and ncRNAs in chloroplasts and mitochondria. Furthermore, Hiten was used to identify the RNA substrates of chloroplast‐ and mitochondrion‐ dual‐localized ZmRNase II and mitochondria‐targeted ZmPPR67. The results show that almost all chloroplast mRNAs and ncRNAs, and mitochondrial atp1 and atp4 mRNAs carry short 3′‐extensions when ZmRNase II is mutated. In the Zmppr67 mutant, 5′ end‐truncated atp9 mRNAs are accumulated, accompanied by a significant reduction in mature atp9 mRNA levels. This study introduces an efficient tool for mapping organellar RNA ends and screening organellar RNA substrates and reveals that ZmRNase II predominantly functions in chloroplast RNA 3′‐end maturation, whereas ZmPPR67 stabilizes mitochondrial atp9 mRNA by protecting its 5′ end.
{"title":"An efficient transcript end mapping tool, Hiten, uncovers the functions of Z m RN ase II and Z m PPR 67 in organellar RNA processing and stability in maize","authors":"Zi‐Wei Qian, Hui Sun, Feng‐Rui Chang, Xun Liao, Lin‐Qu Chen, Xiu‐Chao Lu, Yan‐Yan Wang, Wen‐Xin Liu, Fa‐Qiang Feng, Feng Sun, Bao‐Cai Tan, Ya‐Feng Zhang","doi":"10.1111/nph.70856","DOIUrl":"https://doi.org/10.1111/nph.70856","url":null,"abstract":"Summary <jats:list list-type=\"bullet\"> <jats:list-item> RNA end maturation and stabilization are crucial for plant organellar gene expression, yet the mechanisms remain elusive, partially due to the lack of efficient RNA end mapping methods. </jats:list-item> <jats:list-item> We developed a high‐throughput transcript end mapping tool (Hiten) by integrating <jats:italic>in vitro</jats:italic> RNA circularization, next‐generation sequencing, and circRNA identification algorithm MeCi. </jats:list-item> <jats:list-item> Using Hiten, we systematically mapped 5′ and 3′ ends of organellar mRNAs and noncoding RNAs (ncRNAs) and characterized organellar polyadenosine tails in maize ( <jats:italic>Zea mays</jats:italic> ). Combining RNA 5′‐polyphosphatase treatment with Hiten demonstrates that transcription initiation plays a major role in 5′‐end formation of mRNAs and ncRNAs in chloroplasts and mitochondria. Furthermore, Hiten was used to identify the RNA substrates of chloroplast‐ and mitochondrion‐ dual‐localized ZmRNase II and mitochondria‐targeted ZmPPR67. The results show that almost all chloroplast mRNAs and ncRNAs, and mitochondrial <jats:italic>atp1</jats:italic> and <jats:italic>atp4</jats:italic> mRNAs carry short 3′‐extensions when <jats:italic>ZmRNase II</jats:italic> is mutated. In the <jats:italic>Zmppr67</jats:italic> mutant, 5′ end‐truncated <jats:italic>atp9</jats:italic> mRNAs are accumulated, accompanied by a significant reduction in mature <jats:italic>atp9</jats:italic> mRNA levels. </jats:list-item> <jats:list-item> This study introduces an efficient tool for mapping organellar RNA ends and screening organellar RNA substrates and reveals that ZmRNase II predominantly functions in chloroplast RNA 3′‐end maturation, whereas ZmPPR67 stabilizes mitochondrial <jats:italic>atp9</jats:italic> mRNA by protecting its 5′ end. </jats:list-item> </jats:list>","PeriodicalId":214,"journal":{"name":"New Phytologist","volume":"27 1","pages":""},"PeriodicalIF":9.4,"publicationDate":"2025-12-27","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"145836190","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}
Sara Di Bert, Pascal Benard, Rong Jia, Fabian J. P. Wankmüller, Seren Azad, Anders Kaestner, Andrea Nardini, Timothy J. Brodribb, Andrea Carminati
Summary Understanding when and where drought stress originates in the soil–plant continuum is essential for predicting plant responses to climate change. While stomatal closure is a well‐known reaction to declining soil moisture, the precise hydraulic trigger remains unresolved. We investigated whether the initial reduction in root water uptake is concomitant with a localized depletion of water near the root surface. Using high‐resolution neutron radiography, we visualized dynamic changes in water distribution near maize ( Zea mays L.) roots under controlled drying. We quantified the shift in water uptake patterns and their impact on whole‐plant water use. Under wet conditions, roots primarily extracted water from the bulk soil. As soil moisture declined below a texture‐dependent threshold, hydraulic conductivity dropped, preventing water flow from the bulk soil into the rhizosphere. This caused a shift in water uptake to the rhizosphere, coinciding with reduced transpiration and stomatal downregulation. The transition occurred c . −5 kPa in sandy soils and −200 kPa in loamy soils. These results provide direct evidence that an early hydraulic limitation during soil drying occurs in the rhizosphere, particularly in sandy soils. This redefines the rhizosphere as a dynamic control zone that mediates early drought responses and links microscale hydraulic behavior with whole‐plant function.
{"title":"Early signals of water limitations begin at the root–soil interface: linking rhizosphere drying to water uptake decline","authors":"Sara Di Bert, Pascal Benard, Rong Jia, Fabian J. P. Wankmüller, Seren Azad, Anders Kaestner, Andrea Nardini, Timothy J. Brodribb, Andrea Carminati","doi":"10.1111/nph.70879","DOIUrl":"https://doi.org/10.1111/nph.70879","url":null,"abstract":"Summary <jats:list list-type=\"bullet\"> <jats:list-item> Understanding when and where drought stress originates in the soil–plant continuum is essential for predicting plant responses to climate change. While stomatal closure is a well‐known reaction to declining soil moisture, the precise hydraulic trigger remains unresolved. We investigated whether the initial reduction in root water uptake is concomitant with a localized depletion of water near the root surface. </jats:list-item> <jats:list-item> Using high‐resolution neutron radiography, we visualized dynamic changes in water distribution near maize ( <jats:italic>Zea mays</jats:italic> L.) roots under controlled drying. We quantified the shift in water uptake patterns and their impact on whole‐plant water use. </jats:list-item> <jats:list-item> Under wet conditions, roots primarily extracted water from the bulk soil. As soil moisture declined below a texture‐dependent threshold, hydraulic conductivity dropped, preventing water flow from the bulk soil into the rhizosphere. This caused a shift in water uptake to the rhizosphere, coinciding with reduced transpiration and stomatal downregulation. The transition occurred <jats:italic>c</jats:italic> . −5 kPa in sandy soils and −200 kPa in loamy soils. </jats:list-item> <jats:list-item> These results provide direct evidence that an early hydraulic limitation during soil drying occurs in the rhizosphere, particularly in sandy soils. This redefines the rhizosphere as a dynamic control zone that mediates early drought responses and links microscale hydraulic behavior with whole‐plant function. </jats:list-item> </jats:list>","PeriodicalId":214,"journal":{"name":"New Phytologist","volume":"22 1","pages":""},"PeriodicalIF":9.4,"publicationDate":"2025-12-27","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"145836191","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}
Summary Mass spectrometry imaging (MSI) is an advanced analytical technique that combines mass spectrometry with spatial mapping, enabling the direct, label‐free detection and visualization of molecular distributions within biological tissues. This review comprehensively outlines the fundamental principles, major technological platforms, and recent applications of MSI in plant science. We detail key ionization techniques – matrix‐assisted laser desorption/ionization (MALDI), desorption electrospray ionization (DESI), and secondary ion mass spectrometry (SIMS) – focusing on their ionization mechanisms and instrumental characteristics. We then highlight the transformative impact of MSI in plant research, specifically covering: plant metabolomics, localization of bioactive compounds in medicinal plants, elucidation of plant‐microbe interaction mechanisms, and studies of plant responses to environmental stresses. Finally, we discuss current challenges and future directions for the technology. Due to its high sensitivity, spatial resolution, and label‐free capability, MSI has become a pivotal tool for uncovering plant physiological processes and metabolic regulatory networks, demonstrating significant potential for broad application in plant science.
{"title":"Mass spectrometry imaging: principles and applications in plant research","authors":"Zhixin Liu, Aizhi Qin, Yinpeng Zhang, Qianli Zhao, Mengfan Li, Hao Liu, Yaping Zhou, Mengmeng Zhou, Lulu Yan, Chunyang Li, Luyao Kong, Chun‐Peng Song, Xuwu Sun","doi":"10.1111/nph.70834","DOIUrl":"https://doi.org/10.1111/nph.70834","url":null,"abstract":"Summary Mass spectrometry imaging (MSI) is an advanced analytical technique that combines mass spectrometry with spatial mapping, enabling the direct, label‐free detection and visualization of molecular distributions within biological tissues. This review comprehensively outlines the fundamental principles, major technological platforms, and recent applications of MSI in plant science. We detail key ionization techniques – matrix‐assisted laser desorption/ionization (MALDI), desorption electrospray ionization (DESI), and secondary ion mass spectrometry (SIMS) – focusing on their ionization mechanisms and instrumental characteristics. We then highlight the transformative impact of MSI in plant research, specifically covering: plant metabolomics, localization of bioactive compounds in medicinal plants, elucidation of plant‐microbe interaction mechanisms, and studies of plant responses to environmental stresses. Finally, we discuss current challenges and future directions for the technology. Due to its high sensitivity, spatial resolution, and label‐free capability, MSI has become a pivotal tool for uncovering plant physiological processes and metabolic regulatory networks, demonstrating significant potential for broad application in plant science.","PeriodicalId":214,"journal":{"name":"New Phytologist","volume":"1 1","pages":""},"PeriodicalIF":9.4,"publicationDate":"2025-12-26","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"145829887","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}
Summary Recent experiments show that cryogenic vacuum distillation (CVD) – the standard method for plant water extraction – can introduce biases into δ 2 H measurements of stem water. However, whether similar biases are present in leaf water remains unknown. To test for CVD biases in leaf water, we used an immersion‐based rehydration approach to establish reference water isotope signatures in leaf and stem samples collected from 45 diverse field‐grown species. By comparing isotopic ratios of reference and CVD‐extracted waters, we demonstrate that CVD systematically underestimates leaf water δ 2 H in all species, with magnitudes comparable to those observed in stems. Moreover, the δ 2 H offsets for leaves and stems showed comparable negative correlations with tissue relative water content. By contrast, no CVD‐caused offsets were observed in the control samples (quartz sand and cellulose triacetate) lacking exchangeable organic hydrogen (H). Our study provides the first evidence for the pervasive presence of CVD artifacts in leaf water and identifies deuterium exchange between organic matter and water as the main underlying mechanism. As discussed further, the observed artifacts could have important implications for interpreting fractionation mechanisms that shape δ 2 H values of leaf water and plant organic biomarkers – and thus for isotope‐based ecological and paleoclimatic applications broadly.
{"title":"Cryogenic vacuum distillation‐induced deuterium isotope biases in leaf water and their ecophysiological implications","authors":"Wei Wen, Xianhui Tang, Wen Lin, Yongle Chen, Liguo Zhou, Xin Song","doi":"10.1111/nph.70857","DOIUrl":"https://doi.org/10.1111/nph.70857","url":null,"abstract":"Summary <jats:list list-type=\"bullet\"> <jats:list-item> Recent experiments show that cryogenic vacuum distillation (CVD) – the standard method for plant water extraction – can introduce biases into δ <jats:sup>2</jats:sup> H measurements of stem water. However, whether similar biases are present in leaf water remains unknown. </jats:list-item> <jats:list-item> To test for CVD biases in leaf water, we used an immersion‐based rehydration approach to establish reference water isotope signatures in leaf and stem samples collected from 45 diverse field‐grown species. </jats:list-item> <jats:list-item> By comparing isotopic ratios of reference and CVD‐extracted waters, we demonstrate that CVD systematically underestimates leaf water δ <jats:sup>2</jats:sup> H in all species, with magnitudes comparable to those observed in stems. Moreover, the δ <jats:sup>2</jats:sup> H offsets for leaves and stems showed comparable negative correlations with tissue relative water content. By contrast, no CVD‐caused offsets were observed in the control samples (quartz sand and cellulose triacetate) lacking exchangeable organic hydrogen (H). </jats:list-item> <jats:list-item> Our study provides the first evidence for the pervasive presence of CVD artifacts in leaf water and identifies <jats:italic>deuterium exchange</jats:italic> between organic matter and water as the main underlying mechanism. As discussed further, the observed artifacts could have important implications for interpreting fractionation mechanisms that shape δ <jats:sup>2</jats:sup> H values of leaf water and plant organic biomarkers – and thus for isotope‐based ecological and paleoclimatic applications broadly. </jats:list-item> </jats:list>","PeriodicalId":214,"journal":{"name":"New Phytologist","volume":"46 1","pages":""},"PeriodicalIF":9.4,"publicationDate":"2025-12-26","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"145829886","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":"Was the evolution of faster stomata driven by increased gas exchange rates rather than increasing water use efficiency?","authors":"Robert A. Brench, Matthew J. Wilson, Sarah J. Thorne, Andrew J. Fleming, Julie E. Gray","doi":"10.1111/nph.70830","DOIUrl":"10.1111/nph.70830","url":null,"abstract":"<p>\u0000 </p>","PeriodicalId":214,"journal":{"name":"New Phytologist","volume":"249 5","pages":"2355-2371"},"PeriodicalIF":8.1,"publicationDate":"2025-12-24","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://nph.onlinelibrary.wiley.com/doi/epdf/10.1111/nph.70830","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"145813168","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}
Prasad Parchuri, Sean T. McGuire, Matthew G. Garneau, Niña Alyssa M. Barroga, Philip D. Bates
Plant-derived oils are essential sources of reduced carbon and various fatty acid (FA) structures for food, biofuels, and the oleochemical industry. Despite extensive efforts, engineering mainstream oilseed crops to produce high levels of industrially valuable unusual FAs (UFAs) remains challenging. This review synthesizes recent advances in the understanding of lipid metabolic networks, emphasizing how species-specific regulation of FA synthesis, activation, and delivery influences triacylglycerol (TAG) assembly to govern the efficiency of UFA accumulation. Key insights reveal that acyl flux through anabolic and catabolic branches of lipid metabolism is tightly controlled by enzyme substrate selectivities, diacylglycerol (DAG) pool compartmentalization, and metabolic context, including lipid remodeling and degradation pathways. Engineering success is often constrained by incompatibilities between UFA biosynthetic enzymes and endogenous host metabolism, leading to flux imbalances, futile cycles, and undesired phenotypes. We highlight emerging strategies to overcome these barriers, such as the use of UFA-selective acyltransferases, coordinated manipulation of DAG source pools, suppression of competing endogenous enzymes, and exploitation of TAG remodeling mechanisms. This integrated synthesis provides a conceptual framework for logic-based engineering of oilseeds with enhanced UFA content by offering new avenues for sustainable biomanufacturing of valuable lipids.
{"title":"Understanding the dynamic nature of plant lipid anabolic and catabolic metabolism is key to sustainable oilseed engineering","authors":"Prasad Parchuri, Sean T. McGuire, Matthew G. Garneau, Niña Alyssa M. Barroga, Philip D. Bates","doi":"10.1111/nph.70849","DOIUrl":"10.1111/nph.70849","url":null,"abstract":"<p>Plant-derived oils are essential sources of reduced carbon and various fatty acid (FA) structures for food, biofuels, and the oleochemical industry. Despite extensive efforts, engineering mainstream oilseed crops to produce high levels of industrially valuable unusual FAs (UFAs) remains challenging. This review synthesizes recent advances in the understanding of lipid metabolic networks, emphasizing how species-specific regulation of FA synthesis, activation, and delivery influences triacylglycerol (TAG) assembly to govern the efficiency of UFA accumulation. Key insights reveal that acyl flux through anabolic and catabolic branches of lipid metabolism is tightly controlled by enzyme substrate selectivities, diacylglycerol (DAG) pool compartmentalization, and metabolic context, including lipid remodeling and degradation pathways. Engineering success is often constrained by incompatibilities between UFA biosynthetic enzymes and endogenous host metabolism, leading to flux imbalances, futile cycles, and undesired phenotypes. We highlight emerging strategies to overcome these barriers, such as the use of UFA-selective acyltransferases, coordinated manipulation of DAG source pools, suppression of competing endogenous enzymes, and exploitation of TAG remodeling mechanisms. This integrated synthesis provides a conceptual framework for logic-based engineering of oilseeds with enhanced UFA content by offering new avenues for sustainable biomanufacturing of valuable lipids.</p>","PeriodicalId":214,"journal":{"name":"New Phytologist","volume":"249 5","pages":"2196-2214"},"PeriodicalIF":8.1,"publicationDate":"2025-12-24","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://nph.onlinelibrary.wiley.com/doi/epdf/10.1111/nph.70849","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"145813167","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}
Chase P. Donnelly, Lin Zi, Lingjuan Li, Kris Laukens, Bart Cuypers, Els Prinsen, Mohammed K. Okla, Simon Reynaert, Erik Verbruggen, Han Asard, Gerrit T. S. Beemster, Hamada AbdElgawad
Climate change is leading to more persistent precipitation regimes (PRs) featuring prolonged dry and wet periods in Northern Europe. Plants and plant communities can acclimatize, reducing the impact of repeated exposures to extreme PRs. We addressed the hypothesis that PR adaptations by the soil microbiome contribute to the acclimatization of plants.
We used soils from grassland mesocosms exposed to a 1-d (1SPR) or a 30-d (30SPR) wet/dry cycle to investigate how soil legacy affects the response of four grassland plant species to subsequent PR events.
During the 40-d experiment, 5-d PR (5PR) treatments reduced growth compared with 1-d (1PR) samples, independent of soil legacy. The 30SPR treatment altered soil fungal communities, influencing plant responses, with Plantago and Phleum showing significant stress adaptations when compared with 1SPR. Integrating genome-wide transcriptional, physiological, and biochemical analyses enabled us to propose a mechanistic model showing how soil 30SPR influences four grassland plant species by activating common mechanisms, including redox signaling pathways and stress hormones (jasmonic acid, ethylene, and abscisic acid) under 5PR. These responses lead to cell wall reinforcement through increased lignin and callose, enhancing resilience.
Overall, these findings underscore the role of soil legacy in helping grassland plants adapt to potential future PR variations.
气候变化正在导致北欧出现更多以长时间干湿期为特征的持续降水（pr）。植物和植物群落可以适应，减少反复暴露于极端pr的影响。我们提出了土壤微生物群对PR的适应有助于植物适应环境的假设。我们利用暴露于1 - d （1SPR）或30 - d （30SPR）干湿循环的草地中生态系统土壤，研究土壤遗产如何影响四种草地植物物种对随后的PR事件的响应。在40天的试验中，与1天（1PR）的样品相比，5天的PR （5PR）处理降低了生长，与土壤遗留无关。30SPR处理改变了土壤真菌群落，影响了植物的响应，车前草和车前草与1SPR相比表现出显著的胁迫适应性。整合全基因组转录、生理和生化分析，我们提出了一个机制模型，显示土壤30SPR如何通过激活5PR下的氧化还原信号通路和应激激素（茉莉酸、乙烯和脱落酸）等共同机制影响四种草地植物物种。这些反应通过增加木质素和胼胝质导致细胞壁加强，增强弹性。总的来说，这些发现强调了土壤遗产在帮助草原植物适应潜在的未来PR变化中的作用。
{"title":"The soil microbiome contributes to the adaptation of grassland plant species to increasingly persistent precipitation regimes by inducing transcriptomic, metabolic, and structural changes","authors":"Chase P. Donnelly, Lin Zi, Lingjuan Li, Kris Laukens, Bart Cuypers, Els Prinsen, Mohammed K. Okla, Simon Reynaert, Erik Verbruggen, Han Asard, Gerrit T. S. Beemster, Hamada AbdElgawad","doi":"10.1111/nph.70788","DOIUrl":"10.1111/nph.70788","url":null,"abstract":"<div>\u0000 \u0000 <p>\u0000 </p><ul>\u0000 \u0000 <li>Climate change is leading to more persistent precipitation regimes (PRs) featuring prolonged dry and wet periods in Northern Europe. Plants and plant communities can acclimatize, reducing the impact of repeated exposures to extreme PRs. We addressed the hypothesis that PR adaptations by the soil microbiome contribute to the acclimatization of plants.</li>\u0000 \u0000 <li>We used soils from grassland mesocosms exposed to a 1-d (1SPR) or a 30-d (30SPR) wet/dry cycle to investigate how soil legacy affects the response of four grassland plant species to subsequent PR events.</li>\u0000 \u0000 <li>During the 40-d experiment, 5-d PR (5PR) treatments reduced growth compared with 1-d (1PR) samples, independent of soil legacy. The 30SPR treatment altered soil fungal communities, influencing plant responses, with <i>Plantago</i> and <i>Phleum</i> showing significant stress adaptations when compared with 1SPR. Integrating genome-wide transcriptional, physiological, and biochemical analyses enabled us to propose a mechanistic model showing how soil 30SPR influences four grassland plant species by activating common mechanisms, including redox signaling pathways and stress hormones (jasmonic acid, ethylene, and abscisic acid) under 5PR. These responses lead to cell wall reinforcement through increased lignin and callose, enhancing resilience.</li>\u0000 \u0000 <li>Overall, these findings underscore the role of soil legacy in helping grassland plants adapt to potential future PR variations.</li>\u0000 </ul>\u0000 </div>","PeriodicalId":214,"journal":{"name":"New Phytologist","volume":"249 4","pages":"1937-1953"},"PeriodicalIF":8.1,"publicationDate":"2025-12-23","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"145807666","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}
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