{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,24]],"date-time":"2026-09-24T07:02:21Z","timestamp":1790233341730,"version":"4.1.0"},"reference-count":52,"publisher":"Wiley","license":[{"start":{"date-parts":[[2026,9,23]],"date-time":"2026-09-23T00:00:00Z","timestamp":1790121600000},"content-version":"vor","delay-in-days":0,"URL":"http:\/\/onlinelibrary.wiley.com\/termsAndConditions#vor"},{"start":{"date-parts":[[2026,9,23]],"date-time":"2026-09-23T00:00:00Z","timestamp":1790121600000},"content-version":"tdm","delay-in-days":0,"URL":"http:\/\/doi.wiley.com\/10.1002\/tdm_license_1.1"}],"content-domain":{"domain":["onlinelibrary.wiley.com"],"crossmark-restriction":true},"short-container-title":["Plant Cell &amp; Environment"],"abstract":"<jats:title>ABSTRACT<\/jats:title>\n                  <jats:p>\n                    Rising atmospheric CO\n                    <jats:sub>2<\/jats:sub>\n                    is a defining feature of climate change and profoundly influences plant growth and productivity. While the effects of elevated CO\n                    <jats:sub>2<\/jats:sub>\n                    on photosynthesis and vegetative biomass have been extensively studied, its direct impact on male reproductive development remains poorly understood. Here, we show that elevated CO\n                    <jats:sub>2<\/jats:sub>\n                    improves pollen vigour and performance in tomato (\n                    <jats:italic>Solanum lycopersicum<\/jats:italic>\n                    ). Through genetic and molecular analyses, we identify \u03b2\u2010type carbonic anhydrase 2 (\u03b2CA2) as a pollen\u2010enriched CO\n                    <jats:sub>2<\/jats:sub>\n                    sensor required for this response. Loss of\n                    <jats:italic>\u03b2CA2<\/jats:italic>\n                    abolishes the promoting effects of elevated CO\n                    <jats:sub>2<\/jats:sub>\n                    on fertility, whereas\n                    <jats:italic>\u03b2CA2<\/jats:italic>\n                    overexpression mimics the high\u2010CO\n                    <jats:sub>2<\/jats:sub>\n                    phenotype under ambient conditions. Further analyses revealed that\n                    <jats:italic>\u03b2CA2<\/jats:italic>\n                    regulates downstream networks involved in vesicle trafficking and intracellular transport to promote pollen germination, alongside cellulose and pectin metabolism required for pollen intine remodelling. These findings suggest a potential link between\n                    <jats:italic>\u03b2CA2<\/jats:italic>\n                    \u2010mediated CO\n                    <jats:sub>2<\/jats:sub>\n                    perception, intracellular transport and pollen intine remodelling. Our results uncover a dynamic, pollen\u2010specific CO\n                    <jats:sub>2<\/jats:sub>\n                    response pathway that integrates intracellular transport with structural wall remodelling, providing new insights into how plants sustain male fertility under rising atmospheric CO\n                    <jats:sub>2<\/jats:sub>\n                    .\n                  <\/jats:p>","DOI":"10.1111\/pce.70919","type":"journal-article","created":{"date-parts":[[2026,9,24]],"date-time":"2026-09-24T06:34:14Z","timestamp":1790231654000},"update-policy":"https:\/\/doi.org\/10.1002\/crossmark_policy","source":"Crossref","is-referenced-by-count":0,"title":["A Pollen Carbonic Anhydrase Promotes Male Fertility Under Elevated Carbon Dioxide in Tomato"],"prefix":"10.1111","author":[{"ORCID":"https:\/\/orcid.org\/0009-0006-1077-3615","authenticated-orcid":false,"given":"Jianrong","family":"Lv","sequence":"first","affiliation":[{"name":"Department of Horticulture, College of Agriculture and Biotechnology Zhejiang University Hangzhou China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0009-0005-0662-744X","authenticated-orcid":false,"given":"Haiming","family":"Ying","sequence":"additional","affiliation":[{"name":"Department of Horticulture, College of Agriculture and Biotechnology Zhejiang University Hangzhou China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Chenxin","family":"Yue","sequence":"additional","affiliation":[{"name":"Department of Horticulture, College of Agriculture and Biotechnology Zhejiang University Hangzhou China"},{"name":"Hainan Institute Zhejiang University Sanya China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0009-0007-1533-4352","authenticated-orcid":false,"given":"Zhengran","family":"Zhao","sequence":"additional","affiliation":[{"name":"Department of Horticulture, College of Agriculture and Biotechnology Zhejiang University Hangzhou China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Shurong","family":"Wu","sequence":"additional","affiliation":[{"name":"Department of Horticulture, College of Agriculture and Biotechnology Zhejiang University Hangzhou China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Rui","family":"Deng","sequence":"additional","affiliation":[{"name":"Department of Horticulture, College of Agriculture and Biotechnology Zhejiang University Hangzhou China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Wenshan","family":"Zai","sequence":"additional","affiliation":[{"name":"College of Agriculture and Biotechnology, Wenzhou Vocational College of Science and Technology Wenzhou Zhejiang China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Cunnian","family":"Fu","sequence":"additional","affiliation":[{"name":"College of Agriculture and Biotechnology, Wenzhou Vocational College of Science and Technology Wenzhou Zhejiang China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Huan","family":"Liu","sequence":"additional","affiliation":[{"name":"Department of Horticulture, College of Agriculture and Biotechnology Zhejiang University Hangzhou China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-5989-6989","authenticated-orcid":false,"given":"Christine H.","family":"Foyer","sequence":"additional","affiliation":[{"name":"School of Biosciences, College of Life and Environmental Sciences University of Birmingham Edgbaston UK"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-5351-1910","authenticated-orcid":false,"given":"Kai","family":"Shi","sequence":"additional","affiliation":[{"name":"Department of Horticulture, College of Agriculture and Biotechnology Zhejiang University Hangzhou China"},{"name":"Hainan Institute Zhejiang University Sanya China"},{"name":"Key Laboratory of Horticultural Plants Growth and Development, Ministry of Agriculture and Rural Affairs of China Hangzhou China"},{"name":"Zhejiang Key Laboratory of Horticultural Crop Quality Improvement Hangzhou China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Anran","family":"Wang","sequence":"additional","affiliation":[{"name":"Department of Horticulture, College of Agriculture and Biotechnology Zhejiang University Hangzhou China"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"311","published-online":{"date-parts":[[2026,9,23]]},"reference":[{"key":"e_1_2_9_2_1","doi-asserted-by":"crossref","first-page":"351","DOI":"10.1111\/j.1469-8137.2004.01224.x","article-title":"What Have We Learned From 15 Years of Free\u2010Air CO2 Enrichment (FACE)? A Meta\u2010Analytic Review of the Responses of Photosynthesis, Canopy Properties and Plant Production to Rising CO2","volume":"165","author":"Ainsworth E. A.","year":"2005","journal-title":"New Phytologist"},{"key":"e_1_2_9_3_1","doi-asserted-by":"crossref","first-page":"437","DOI":"10.1146\/annurev-arplant-042809-112312","article-title":"Genetic Regulation of Sporopollenin Synthesis and Pollen Exine Development","volume":"62","author":"Ariizumi T.","year":"2011","journal-title":"Annual Review of Plant Biology"},{"key":"e_1_2_9_4_1","doi-asserted-by":"crossref","first-page":"1465","DOI":"10.1093\/jxb\/ern355","article-title":"Male Gametophyte Development: A Molecular Perspective","volume":"60","author":"Borg M.","year":"2009","journal-title":"Journal of Experimental Botany"},{"key":"e_1_2_9_5_1","doi-asserted-by":"crossref","first-page":"6213","DOI":"10.1111\/pce.15599","article-title":"Trehalose\u20106\u2010Phosphate Phosphatase SlTPP1 Adjusts Diurnal Carbohydrate Partitioning in Tomato","volume":"48","author":"Chai L.","year":"2025","journal-title":"Plant, Cell & Environment"},{"key":"e_1_2_9_6_1","doi-asserted-by":"crossref","first-page":"571","DOI":"10.1111\/nph.17380","article-title":"Heat Stress Response Mechanisms in Pollen Development","volume":"231","author":"Chaturvedi P.","year":"2021","journal-title":"New Phytologist"},{"key":"e_1_2_9_7_1","doi-asserted-by":"crossref","first-page":"37","DOI":"10.1111\/tpj.16207","article-title":"Full\u2010Length EFOP3 and EFOP4 Proteins Are Essential for Pollen Intine Development in Arabidopsis thaliana","volume":"115","author":"Chen X.","year":"2023","journal-title":"Plant Journal"},{"key":"e_1_2_9_8_1","doi-asserted-by":"crossref","first-page":"3498","DOI":"10.1093\/plcell\/koae163","article-title":"The Brassinosteroid Receptor StBRI1 Promotes Tuber Development by Enhancing Plasma Membrane H+\u2010ATPase Activity in Potato","volume":"36","author":"Deng R.","year":"2024","journal-title":"Plant Cell"},{"key":"e_1_2_9_9_1","doi-asserted-by":"crossref","first-page":"30","DOI":"10.1016\/j.molp.2016.09.001","article-title":"Plant Carbonic Anhydrases: Structures, Locations, Evolution, and Physiological Roles","volume":"10","author":"DiMario R. J.","year":"2017","journal-title":"Molecular Plant"},{"key":"e_1_2_9_10_1","doi-asserted-by":"crossref","first-page":"216","DOI":"10.1104\/pp.17.01722","article-title":"The ADAPTOR PROTEIN\u20103 Complex Mediates Pollen Tube Growth by Coordinating Vacuolar Targeting and Organization","volume":"177","author":"Feng Q. N.","year":"2018","journal-title":"Plant Physiology"},{"key":"e_1_2_9_11_1","doi-asserted-by":"crossref","DOI":"10.1098\/rstb.2024.0247","article-title":"CO2 Signalling in Plants","volume":"380","author":"Foyer C.","year":"2025","journal-title":"Philosophical Transactions of the Royal Society, B: Biological Sciences"},{"key":"e_1_2_9_12_1","doi-asserted-by":"crossref","first-page":"64","DOI":"10.1016\/j.ydbio.2016.07.023","article-title":"Plant Developmental Responses to Climate Change","volume":"419","author":"Gray S. B.","year":"2016","journal-title":"Developmental Biology"},{"key":"e_1_2_9_13_1","doi-asserted-by":"crossref","DOI":"10.1016\/j.celrep.2026.117131","article-title":"Phytochrome B Modulates High\u2010Temperature\u2010Induced Flowering in Soybean by Promoting Degradation of PSEUDO\u2010RESPONSE REGULATOR 5 Proteins","volume":"45","author":"Hou Z.","year":"2026","journal-title":"Cell Reports"},{"key":"e_1_2_9_14_1","doi-asserted-by":"crossref","first-page":"87","DOI":"10.1038\/ncb2009","article-title":"Carbonic Anhydrases Are Upstream Regulators of CO2\u2010Controlled Stomatal Movements in Guard Cells","volume":"12","author":"Hu H.","year":"2010","journal-title":"Nature Cell Biology"},{"key":"e_1_2_9_15_1","doi-asserted-by":"crossref","first-page":"2827","DOI":"10.1111\/nph.17087","article-title":"High CO2\u2010 and Pathogen\u2010Driven Expression of the Carbonic Anhydrase \u03b2CA3 Confers Basal Immunity in Tomato","volume":"229","author":"Hu Z.","year":"2021","journal-title":"New Phytologist"},{"key":"e_1_2_9_16_1","doi-asserted-by":"crossref","first-page":"1335","DOI":"10.1105\/tpc.16.00484","article-title":"Carbonic Anhydrases Function in Anther Cell Differentiation Downstream of the Receptor\u2010Like Kinase EMS1","volume":"29","author":"Huang J.","year":"2017","journal-title":"Plant Cell"},{"key":"e_1_2_9_17_1","doi-asserted-by":"crossref","first-page":"9","DOI":"10.1046\/j.1469-8137.2002.00494.x","article-title":"Plant Reproduction Under Elevated CO2 Conditions: A Meta\u2010Analysis of Reports on 79 Crop and Wild Species","volume":"156","author":"Jablonski L. M.","year":"2002","journal-title":"New Phytologist"},{"key":"e_1_2_9_18_1","doi-asserted-by":"crossref","DOI":"10.3389\/fpls.2021.703713","article-title":"Sequential Deposition and Remodeling of Cell Wall Polymers During Tomato Pollen Development","volume":"12","author":"Jaffri S. R. F.","year":"2021","journal-title":"Frontiers in Plant Science"},{"key":"e_1_2_9_19_1","doi-asserted-by":"crossref","first-page":"1630","DOI":"10.1093\/mp\/sst067","article-title":"Rice Male Development Under Drought Stress: Phenotypic Changes and Stage\u2010Dependent Transcriptomic Reprogramming","volume":"6","author":"Jin Y.","year":"2013","journal-title":"Molecular Plant"},{"key":"e_1_2_9_20_1","doi-asserted-by":"crossref","first-page":"725","DOI":"10.1093\/jxb\/eri044","article-title":"Interactive Effects of Carbon Dioxide, Temperature, and Ultraviolet\u2010B Radiation on Soybean (Glycine max L.) Flower and Pollen Morphology, Pollen Production, Germination, and Tube Lengths","volume":"56","author":"Koti S.","year":"2005","journal-title":"Journal of Experimental Botany"},{"key":"e_1_2_9_21_1","doi-asserted-by":"crossref","first-page":"112","DOI":"10.3390\/plants4010112","article-title":"Cell Wall Metabolism in Response to Abiotic Stress","volume":"4","author":"Le Gall H.","year":"2015","journal-title":"Plants"},{"key":"e_1_2_9_22_1","doi-asserted-by":"crossref","first-page":"2859","DOI":"10.1093\/jxb\/erp096","article-title":"Elevated CO2 Effects on Plant Carbon, Nitrogen, and Water Relations: Six Important Lessons From FACE","volume":"60","author":"Leakey A. D. B.","year":"2009","journal-title":"Journal of Experimental Botany"},{"key":"e_1_2_9_23_1","unstructured":"Lee H. K.Calvin andD.Dasgupta et al.2023.Climate Change 2023: Synthesis Report. Intergovernmental Panel on Climate Change."},{"key":"e_1_2_9_24_1","doi-asserted-by":"crossref","first-page":"367","DOI":"10.1104\/pp.114.250928","article-title":"PECTIN METHYLESTERASE48 Is Involved in Arabidopsis Pollen Grain Germination","volume":"167","author":"Leroux C.","year":"2015","journal-title":"Plant Physiology"},{"key":"e_1_2_9_25_1","doi-asserted-by":"crossref","first-page":"3152","DOI":"10.1111\/pbi.70142","article-title":"Dt1 Interacts With HB40 to Affect Lateral Root Primordium Development by Regulating CDC48 in Soybean","volume":"23","author":"Li H.","year":"2025","journal-title":"Plant Biotechnology Journal"},{"key":"e_1_2_9_26_1","doi-asserted-by":"crossref","first-page":"185","DOI":"10.1073\/pnas.1118560109","article-title":"Cellulose Synthase Interactive Protein 1 (CSI1) Links Microtubules and Cellulose Synthase Complexes","volume":"109","author":"Li S.","year":"2012","journal-title":"Proceedings of the National Academy of Sciences"},{"key":"e_1_2_9_27_1","doi-asserted-by":"crossref","first-page":"1149","DOI":"10.1111\/pce.15192","article-title":"Phosphorylation of ADF7\u2010Mediated by AGC1.7 Regulates Pollen Germination in Arabidopsis thaliana","volume":"48","author":"Li X.","year":"2025","journal-title":"Plant, Cell & Environment"},{"key":"e_1_2_9_28_1","doi-asserted-by":"crossref","DOI":"10.1080\/15592324.2018.1464854","article-title":"Vacuolar Trafficking in Pollen Tube Growth and Guidance","volume":"13","author":"Liang X.","year":"2018","journal-title":"Plant Signaling & Behavior"},{"key":"e_1_2_9_29_1","doi-asserted-by":"crossref","first-page":"1918","DOI":"10.1126\/science.1114722","article-title":"Food for Thought: Lower\u2010Than\u2010Expected Crop Yield Stimulation With Rising CO2 Concentrations","volume":"312","author":"Long S. P.","year":"2006","journal-title":"Science"},{"key":"e_1_2_9_30_1","doi-asserted-by":"crossref","DOI":"10.1016\/j.xplc.2026.101818","article-title":"PSKR1\u2010Mediated Phosphorylation of \u03b2CA2 Activates Its Carbonic Anhydrase Activity to Integrate CO2 and Heat Signals for Enhanced Thermotolerance in Tomato","volume":"7","author":"Lv J.","year":"2026","journal-title":"Plant Communications"},{"key":"e_1_2_9_31_1","doi-asserted-by":"crossref","first-page":"3843","DOI":"10.1093\/jxb\/ers077","article-title":"Effect of Elevated CO2 and High Temperature on Seed\u2010Set and Grain Quality of Rice","volume":"63","author":"Madan P.","year":"2012","journal-title":"Journal of Experimental Botany"},{"key":"e_1_2_9_32_1","doi-asserted-by":"crossref","first-page":"325","DOI":"10.1007\/s00497-010-0146-8","article-title":"Pollen Performance of Raphanus sativus (Brassicaceae) Declines in Response to Elevated [CO2]","volume":"23","author":"Marshall D. L.","year":"2010","journal-title":"Sexual Plant Reproduction"},{"key":"e_1_2_9_33_1","doi-asserted-by":"crossref","first-page":"S142","DOI":"10.1105\/tpc.016659","article-title":"Control of Male Gametophyte Development","volume":"16","author":"McCormick S.","year":"2004","journal-title":"Plant Cell"},{"key":"e_1_2_9_34_1","doi-asserted-by":"crossref","first-page":"141","DOI":"10.1111\/j.1365-3040.2001.00669.x","article-title":"Carbonic Anhydrases in Plants and Algae","volume":"24","author":"Moroney J. 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V.","year":"2006","journal-title":"Agricultural and Forest Meteorology"},{"key":"e_1_2_9_38_1","doi-asserted-by":"crossref","first-page":"1775","DOI":"10.1046\/j.1365-2486.2003.00708.x","article-title":"Super\u2010Optimal Temperatures Are Detrimental to Peanut (Arachis hypogaea L.) Reproductive Processes and Yield at Both Ambient and Elevated Carbon Dioxide","volume":"9","author":"Prasad P. V. V.","year":"2003","journal-title":"Global Change Biology"},{"key":"e_1_2_9_39_1","doi-asserted-by":"crossref","first-page":"1187","DOI":"10.1093\/jexbot\/53.371.1187","article-title":"Determining Critical Pre\u2010 and Post\u2010Anthesis Periods and Physiological Processes in Lycopersicon esculentum Mill. Exposed to Moderately Elevated Temperatures","volume":"53","author":"Sato S.","year":"2002","journal-title":"Journal of Experimental Botany"},{"key":"e_1_2_9_40_1","doi-asserted-by":"crossref","first-page":"963","DOI":"10.1104\/pp.49.6.963","article-title":"Pollen Germination and Tube Growth: Dependent on Carbon Dioxide and Independent of Ethylene","volume":"49","author":"Sfakiotakis E. M.","year":"1972","journal-title":"Plant Physiology"},{"key":"e_1_2_9_41_1","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1111\/pce.12142","article-title":"The Impact of Environmental Stress on Male Reproductive Development in Plants: Biological Processes and Molecular Mechanisms","volume":"37","author":"Storme N. 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N.","year":"2022","journal-title":"Plant Physiology"},{"key":"e_1_2_9_49_1","doi-asserted-by":"crossref","first-page":"11259","DOI":"10.1073\/pnas.0800036105","article-title":"Novelties of the Flowering Plant Pollen Tube Underlie Diversification of a Key Life History Stage","volume":"105","author":"Williams J. H.","year":"2008","journal-title":"Proceedings of the National Academy of Sciences"},{"key":"e_1_2_9_50_1","doi-asserted-by":"crossref","first-page":"6704","DOI":"10.1111\/pce.15645","article-title":"G\u03b1 Protein Mediates High\u2010Concentration CO2\u2010Induced Stomata Closure Through Interaction With Carbonic Anhydrase to Promote Guard Cell Hydrogen Peroxide Production in Arabidopsis","volume":"48","author":"Zhang C. 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