{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,19]],"date-time":"2026-10-19T00:39:22Z","timestamp":1792370362668,"version":"4.4.0"},"reference-count":44,"publisher":"Wiley","issue":"5","license":[{"start":{"date-parts":[[2026,10,18]],"date-time":"2026-10-18T00:00:00Z","timestamp":1792281600000},"content-version":"vor","delay-in-days":47,"URL":"http:\/\/creativecommons.org\/licenses\/by\/4.0\/"},{"start":{"date-parts":[[2026,9,1]],"date-time":"2026-09-01T00:00:00Z","timestamp":1788220800000},"content-version":"tdm","delay-in-days":0,"URL":"http:\/\/doi.wiley.com\/10.1002\/tdm_license_1.1"}],"funder":[{"DOI":"10.13039\/501100001807","name":"Funda\u00e7\u00e3o de Amparo \u00e0 Pesquisa do Estado de S\u00e3o Paulo","doi-asserted-by":"publisher","award":["2024\/21237\u20103"],"award-info":[{"award-number":["2024\/21237\u20103"]}],"id":[{"id":"10.13039\/501100001807","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100001807","name":"Funda\u00e7\u00e3o de Amparo \u00e0 Pesquisa do Estado de S\u00e3o Paulo","doi-asserted-by":"publisher","award":["2025\/20086\u20104"],"award-info":[{"award-number":["2025\/20086\u20104"]}],"id":[{"id":"10.13039\/501100001807","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100003593","name":"Conselho Nacional de Desenvolvimento Cient\u00edfico e Tecnol\u00f3gico","doi-asserted-by":"publisher","award":["301453\/2022\u20105"],"award-info":[{"award-number":["301453\/2022\u20105"]}],"id":[{"id":"10.13039\/501100003593","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["onlinelibrary.wiley.com"],"crossmark-restriction":true},"short-container-title":["Physiologia Plantarum"],"published-print":{"date-parts":[[2026,9]]},"abstract":"<jats:title>ABSTRACT<\/jats:title>\n                  <jats:p>\n                    Asymmetric warming, characterized by faster increases in nighttime than daytime temperatures, is an emerging threat to crop performance. However, the interactive physiological effects of day versus night heat remain insufficiently resolved in soybean (\n                    <jats:styled-content style=\"fixed-case\">\n                      <jats:italic>Glycine max<\/jats:italic>\n                    <\/jats:styled-content>\n                    L. Merr.). Here, we evaluated soybean responses to 4\u2009day\/night thermal regimes (28\u00b0C\/22\u00b0C, 40\u00b0C\/22\u00b0C, 28\u00b0C\/28\u00b0C, and 40\u00b0C\/28\u00b0C) to test whether nighttime warming is the dominant driver of stress disruption. Isolated daytime heat (40\u00b0C\/22\u00b0C) enhanced photosynthetic performance and maintained biomass, indicating short\u2010term functional plasticity. In contrast, treatments including elevated nighttime temperature impaired pre\u2010dawn rehydration, reduced leaf water status, and intensified membrane damage, with the strongest effects under combined heat (40\u00b0C\/28\u00b0C). Combined stress also caused severe stomatal limitation of CO\n                    <jats:sub>2<\/jats:sub>\n                    assimilation, depletion of soluble sugars, accumulation of proline and glycine betaine, and strong activation of antioxidant enzymes accompanied by high H\n                    <jats:sub>2<\/jats:sub>\n                    O\n                    <jats:sub>2<\/jats:sub>\n                    and TBARS levels, indicating that oxidative load exceeded detoxification capacity. Multivariate integration reinforced this pattern by clearly separating combined heat from all other treatments and placing nighttime warming as the central axis of physiological disruption. Together, our findings demonstrate that restricted nocturnal recovery is a key mechanism underlying synergistic damage under sustained day\u2013night heat, highlighting nighttime metabolism and overnight hydraulic recovery as priority targets for improving soybean heat resilience.\n                  <\/jats:p>","DOI":"10.1111\/ppl.71100","type":"journal-article","created":{"date-parts":[[2026,10,18]],"date-time":"2026-10-18T23:40:56Z","timestamp":1792366856000},"update-policy":"https:\/\/doi.org\/10.1002\/crossmark_policy","source":"Crossref","is-referenced-by-count":0,"title":["Combined Day\u2013Night Heat Damage in Soybean Is Driven by Nighttime Warming"],"prefix":"10.1111","volume":"178","author":[{"given":"Gabriel Ferraz","family":"Guimar\u00e3es","sequence":"first","affiliation":[{"name":"Institute of Biosciences, Department of Biological and Environmental Sciences, Laboratory of Plant Metabolism S\u00e3o Paulo State University (UNESP)  S\u00e3o\u00a0Vicente SP Brazil"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"J\u00e9ssica de Jesus","family":"Santos","sequence":"additional","affiliation":[{"name":"Institute of Biosciences, Department of Biological and Environmental Sciences, Laboratory of Plant Metabolism S\u00e3o Paulo State University (UNESP)  S\u00e3o\u00a0Vicente SP Brazil"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Rafael Vasconcelos","family":"Ribeiro","sequence":"additional","affiliation":[{"name":"Institute of Biology (IB), Department of Plant Biology, Laboratory of Crop Physiology State University of Campinas (UNICAMP)  Campinas SP Brazil"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-8867-7301","authenticated-orcid":false,"given":"Milton Costa","family":"Lima Neto","sequence":"additional","affiliation":[{"name":"Institute of Biosciences, Department of Biological and Environmental Sciences, Laboratory of Plant Metabolism S\u00e3o Paulo State University (UNESP)  S\u00e3o\u00a0Vicente SP Brazil"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"311","published-online":{"date-parts":[[2026,10,18]]},"reference":[{"key":"e_1_2_11_2_1","doi-asserted-by":"crossref","DOI":"10.1016\/j.envexpbot.2024.105871","article-title":"Exploring the Coordinated Hydraulic Plasticity Across Organs in Soybean Plants Exposed to Drought Cycles","volume":"226","author":"Alves R. D. F. B.","year":"2024","journal-title":"Environmental and Experimental Botany"},{"issue":"1","key":"e_1_2_11_3_1","doi-asserted-by":"crossref","first-page":"205","DOI":"10.1007\/BF00018060","article-title":"Rapid Determination of Free Proline for Water\u2010Stress Studies","volume":"39","author":"Bates L. S.","year":"1973","journal-title":"Plant and Soil"},{"issue":"1","key":"e_1_2_11_4_1","doi-asserted-by":"crossref","first-page":"248","DOI":"10.1016\/0003-2697(76)90527-3","article-title":"A Rapid and Sensitive Method for the Quantitation of Microgram Quantities of Protein Utilizing the Principle of Protein\u2010Dye Binding","volume":"72","author":"Bradford M. M.","year":"1976","journal-title":"Analytical Biochemistry"},{"key":"e_1_2_11_5_1","doi-asserted-by":"publisher","DOI":"10.1111\/tpj.14674"},{"issue":"9","key":"e_1_2_11_6_1","doi-asserted-by":"crossref","first-page":"3344","DOI":"10.1111\/pce.14815","article-title":"A Guide to Photosynthetic Gas Exchange Measurements: Fundamental Principles, Best Practice and Potential Pitfalls","volume":"47","author":"Busch F. A.","year":"2024","journal-title":"Plant, Cell & Environment"},{"issue":"3","key":"e_1_2_11_7_1","doi-asserted-by":"crossref","first-page":"463","DOI":"10.1111\/j.1399-3054.1991.tb00121.x","article-title":"Effect of Aluminium on Lipid Peroxidation, Superoxide Dismutase, Catalase, and Peroxidase Activities in Root Tips of Two Wheat Cultivars","volume":"83","author":"Cakmak I.","year":"1991","journal-title":"Physiologia Plantarum"},{"key":"e_1_2_11_8_1","doi-asserted-by":"crossref","DOI":"10.1016\/j.plaphy.2025.109681","article-title":"Physiological and Biochemical Changes Associated With the Induction of Facultative CAM in \n                     Pereskia aculeata\n                   Under Drought Stress and Recovery","volume":"222","author":"Cenciareli L. C.","year":"2025","journal-title":"Plant Physiology and Biochemistry"},{"issue":"1","key":"e_1_2_11_9_1","doi-asserted-by":"crossref","first-page":"79","DOI":"10.1002\/joc.4688","article-title":"Diurnal Asymmetry to the Observed Global Warming","volume":"37","author":"Davy R.","year":"2016","journal-title":"International Journal of Climatology"},{"key":"e_1_2_11_10_1","doi-asserted-by":"crossref","DOI":"10.3389\/fpls.2023.1332414","article-title":"Optimization of Soybean Physiochemical, Agronomic, and Genetic Responses Under Varying Regimes of Day and Night Temperatures","volume":"14","author":"Ding C.","year":"2024","journal-title":"Frontiers in Plant Science"},{"issue":"5","key":"e_1_2_11_11_1","doi-asserted-by":"crossref","first-page":"2125","DOI":"10.2135\/cropsci2010.10.0571","article-title":"High\u2010Temperature Stress and Soybean Leaves: Leaf Anatomy and Photosynthesis","volume":"51","author":"Djanaguiraman M.","year":"2011","journal-title":"Crop Science"},{"issue":"4","key":"e_1_2_11_12_1","doi-asserted-by":"crossref","first-page":"1594","DOI":"10.2135\/cropsci2012.07.0441","article-title":"High Day\u2010 Or Nighttime Temperature Alters Leaf Assimilation, Reproductive Success, and Phosphatidic Acid of Pollen Grain in Soybean [\n                     Glycine max\n                   (L.) Merr.]","volume":"53","author":"Djanaguiraman M.","year":"2013","journal-title":"Crop Science"},{"issue":"2","key":"e_1_2_11_13_1","doi-asserted-by":"crossref","first-page":"309","DOI":"10.1104\/pp.59.2.309","article-title":"Superoxide Dismutases: I. Occurrence in Higher Plants","volume":"59","author":"Giannopolitis C. N.","year":"1977","journal-title":"Plant Physiology"},{"issue":"12","key":"e_1_2_11_14_1","doi-asserted-by":"crossref","first-page":"909","DOI":"10.1016\/j.plaphy.2010.08.016","article-title":"Reactive Oxygen Species and Antioxidant Machinery in Abiotic Stress Tolerance in Crop Plants","volume":"48","author":"Gill S. S.","year":"2010","journal-title":"Plant Physiology and Biochemistry"},{"key":"e_1_2_11_15_1","doi-asserted-by":"crossref","DOI":"10.1016\/j.fcr.2025.110142","article-title":"Nighttime Warming Affects Yields of Major Grain Crops: A Global Meta\u2010Analysis","volume":"334","author":"Gim\u00e9nez V. D.","year":"2025","journal-title":"Field Crops Research"},{"issue":"2","key":"e_1_2_11_16_1","doi-asserted-by":"crossref","DOI":"10.1007\/BF02374789","article-title":"Rapid Assay for Determination of Water Soluble Quaternary Ammonium Compounds","volume":"70","author":"Grieve C. M.","year":"1983","journal-title":"Plant and Soil"},{"issue":"2","key":"e_1_2_11_17_1","doi-asserted-by":"crossref","first-page":"450","DOI":"10.1104\/pp.84.2.450","article-title":"Biochemical and Developmental Characterization of Multiple Forms of Catalase in Tobacco Leaves","volume":"84","author":"Havir E. A.","year":"1987","journal-title":"Plant Physiology"},{"key":"e_1_2_11_18_1","doi-asserted-by":"crossref","DOI":"10.3389\/fpls.2020.00153","article-title":"Characterization of Photosynthetic Phenotypes and Chloroplast Ultrastructural Changes of Soybean (\n                     Glycine max\n                  ) in Response to Elevated Air Temperatures","volume":"11","author":"Herritt M. T.","year":"2020","journal-title":"Frontiers in Plant Science"},{"key":"e_1_2_11_19_1","volume-title":"The Water Culture Method for Growing Plants Without Soil","author":"Hoagland D. R.","year":"1950"},{"issue":"3","key":"e_1_2_11_20_1","doi-asserted-by":"crossref","DOI":"10.1088\/1748-9326\/3\/3\/034003","article-title":"Impacts of Recent Climate Change on Wisconsin Corn and Soybean Yield Trends","volume":"3","author":"Kucharik C. J.","year":"2008","journal-title":"Environmental Research Letters"},{"key":"e_1_2_11_21_1","doi-asserted-by":"crossref","DOI":"10.3390\/atmos15040392","article-title":"Quantifying High\u2010Temperature and Drought Stress Effects on Soybean Growth and Yield in the Western Guanzhong Plain","volume":"15","author":"Li M.","year":"2024","journal-title":"Atmosphere"},{"key":"e_1_2_11_22_1","doi-asserted-by":"crossref","first-page":"350","DOI":"10.1016\/0076-6879(87)48036-1","article-title":"Chlorophylls and Carotenoids: Pigments of Photosynthetic Biomembranes","volume":"148","author":"Lichtenthaler H. K.","year":"1987","journal-title":"Methods in Enzymology"},{"issue":"4","key":"e_1_2_11_23_1","doi-asserted-by":"crossref","first-page":"650","DOI":"10.1111\/plb.12573","article-title":"Cyclic Electron Flow, NPQ and Photorespiration Are Crucial for the Establishment of Young Plants of \n                     Ricinus communis\n                   and \n                     Jatropha curcas\n                   Exposed to Drought","volume":"19","author":"Lima Neto M. C.","year":"2017","journal-title":"Plant Biology"},{"issue":"3","key":"e_1_2_11_24_1","doi-asserted-by":"crossref","first-page":"267","DOI":"10.1080\/1343943X.2020.1842215","article-title":"The Influence of High Night Temperature on Yield and Physiological Attributes of Soybean cv. Fukuyutaka","volume":"24","author":"Lin T. Y.","year":"2021","journal-title":"Plant Production Science"},{"issue":"4","key":"e_1_2_11_25_1","doi-asserted-by":"crossref","first-page":"2597","DOI":"10.1002\/joc.6978","article-title":"Evidence of Asymmetric Change in Diurnal Temperature Range in Recent Decades Over Different Agro\u2010Climatic Zones of India","volume":"41","author":"Mall R. K.","year":"2021","journal-title":"International Journal of Climatology"},{"key":"e_1_2_11_26_1","doi-asserted-by":"publisher","DOI":"10.1093\/jxb\/erab090"},{"issue":"13","key":"e_1_2_11_27_1","doi-asserted-by":"crossref","first-page":"3983","DOI":"10.1093\/jxb\/ert208","article-title":"Chlorophyll Fluorescence Analysis: A Guide to Good Practice and Understanding Some New Applications","volume":"64","author":"Murchie E. H.","year":"2013","journal-title":"Journal of Experimental Botany"},{"issue":"2","key":"e_1_2_11_28_1","doi-asserted-by":"crossref","first-page":"98","DOI":"10.2480\/agrmet.D-14-00046","article-title":"Evaluation of the Effects of Increasing Temperature on the Transpiration Rate and Canopy Conductance of Soybean by Using the Sap Flow Method","volume":"71","author":"Nakano S.","year":"2015","journal-title":"Journal of Agricultural Meteorology"},{"issue":"5","key":"e_1_2_11_29_1","doi-asserted-by":"crossref","first-page":"867","DOI":"10.1093\/oxfordjournals.pcp.a076232","article-title":"Hydrogen Peroxide Is Scavenged by Ascorbate\u2010Specific Peroxidase in Spinach Chloroplasts","volume":"22","author":"Nakano Y.","year":"1981","journal-title":"Plant and Cell Physiology"},{"issue":"6","key":"e_1_2_11_30_1","doi-asserted-by":"crossref","first-page":"425","DOI":"10.1007\/s10863-018-9783-7","article-title":"Thylakoid Membrane Unstacking Increases LHCII Thermal Stability and Lipid Phase Fluidity","volume":"50","author":"Petrova N.","year":"2018","journal-title":"Journal of Bioenergetics and Biomembranes"},{"key":"e_1_2_11_31_1","volume-title":"R: A Language and Environment for Statistical Computing","author":"R Core Team","year":"2024"},{"key":"e_1_2_11_32_1","doi-asserted-by":"publisher","DOI":"10.1590\/1678\u20104499.0146"},{"key":"e_1_2_11_33_1","doi-asserted-by":"crossref","DOI":"10.1016\/j.stress.2025.100826","article-title":"High Night Temperature Disrupts the Assimilate Utilization and Yield Potential in Soybean","volume":"16","author":"Sankarapillai L. V.","year":"2025","journal-title":"Plant Stress"},{"issue":"3668","key":"e_1_2_11_34_1","doi-asserted-by":"crossref","first-page":"339","DOI":"10.1126\/science.148.3668.339","article-title":"Sap pressure in vascular plants","volume":"148","author":"Scholander P. F.","year":"1965","journal-title":"Science"},{"key":"e_1_2_11_35_1","doi-asserted-by":"crossref","DOI":"10.1016\/j.stress.2024.100725","article-title":"Revolutionizing Heat Stress Tolerance in \n                     Glycine max\n                  : Exploring the Latest Advances in Microbial Application","volume":"15","author":"Shaffique S.","year":"2024","journal-title":"Plant Stress"},{"issue":"8","key":"e_1_2_11_36_1","doi-asserted-by":"crossref","first-page":"3114","DOI":"10.1111\/gcb.12935","article-title":"Heat Waves Imposed During Early Pod Development in Soybean (\n                     Glycine max\n                  ) Cause Significant Yield Loss Despite a Rapid Recovery From Oxidative Stress","volume":"21","author":"Siebers M. H.","year":"2015","journal-title":"Global Change Biology"},{"issue":"10","key":"e_1_2_11_37_1","doi-asserted-by":"crossref","first-page":"2750","DOI":"10.1111\/pce.13572","article-title":"Carbon Assimilation in Crops at High Temperatures","volume":"42","author":"Slattery R. A.","year":"2019","journal-title":"Plant, Cell & Environment"},{"key":"e_1_2_11_38_1","doi-asserted-by":"crossref","DOI":"10.1186\/1471-2229-14-111","article-title":"Effects of High Temperature on Photosynthesis and Related Gene Expression in Poplar","volume":"14","author":"Song Y.","year":"2014","journal-title":"BMC Plant Biology"},{"key":"e_1_2_11_39_1","doi-asserted-by":"crossref","DOI":"10.3389\/fpls.2024.1427086","article-title":"Temperature and Elevated CO2 Alter Soybean Seed Yield and Quality, Exhibiting Transgenerational Effects on Seedling Emergence and Vigor","volume":"15","author":"Thenveettil N.","year":"2024","journal-title":"Frontiers in Plant Science"},{"issue":"3","key":"e_1_2_11_40_1","doi-asserted-by":"crossref","first-page":"199","DOI":"10.1016\/j.envexpbot.2007.05.011","article-title":"Heat Tolerance in Plants: An Overview","volume":"61","author":"Wahid A.","year":"2007","journal-title":"Environmental and Experimental Botany"},{"key":"e_1_2_11_41_1","doi-asserted-by":"publisher","DOI":"10.1023\/A:1005884717655"},{"key":"e_1_2_11_42_1","doi-asserted-by":"crossref","DOI":"10.3389\/fpls.2023.1065604","article-title":"Effects of High Night Temperature on Soybean Yield and Compositions","volume":"14","author":"Yang L.","year":"2023","journal-title":"Frontiers in Plant Science"},{"issue":"3","key":"e_1_2_11_43_1","doi-asserted-by":"crossref","first-page":"508","DOI":"10.1042\/bj0570508","article-title":"The Estimation of Carbohydrates in Plant Extracts by Anthrone","volume":"57","author":"Yemm E. W.","year":"1954","journal-title":"Biochemical Journal"},{"issue":"5","key":"e_1_2_11_44_1","doi-asserted-by":"crossref","first-page":"569","DOI":"10.1017\/S002185960900879X","article-title":"The Effects of Global Warming on Soybean Yields in a Long\u2010Term Fertilization Experiment in Northeast China","volume":"147","author":"Zheng H. F.","year":"2009","journal-title":"Journal of Agricultural Science"},{"issue":"2","key":"e_1_2_11_45_1","doi-asserted-by":"crossref","first-page":"162","DOI":"10.1006\/abio.1997.2391","article-title":"A Stable Nonfluorescent Derivative of Resorufin for the Fluorometric Determination of Horseradish Peroxidase Activity","volume":"253","author":"Zhou M.","year":"1997","journal-title":"Analytical Biochemistry"}],"container-title":["Physiologia Plantarum"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/onlinelibrary.wiley.com\/doi\/pdf\/10.1111\/ppl.71100","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/onlinelibrary.wiley.com\/doi\/full-xml\/10.1111\/ppl.71100","content-type":"application\/xml","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/onlinelibrary.wiley.com\/doi\/pdf\/10.1111\/ppl.71100","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2026,10,18]],"date-time":"2026-10-18T23:41:02Z","timestamp":1792366862000},"score":1,"resource":{"primary":{"URL":"https:\/\/onlinelibrary.wiley.com\/doi\/10.1111\/ppl.71100"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2026,9]]},"references-count":44,"journal-issue":{"issue":"5","published-print":{"date-parts":[[2026,9]]}},"alternative-id":["10.1111\/ppl.71100"],"URL":"https:\/\/doi.org\/10.1111\/ppl.71100","archive":["Portico"],"relation":{},"ISSN":["0031-9317","1399-3054"],"issn-type":[{"value":"0031-9317","type":"print"},{"value":"1399-3054","type":"electronic"}],"subject":[],"published":{"date-parts":[[2026,9]]},"assertion":[{"value":"2026-07-12","order":0,"name":"received","label":"Received","group":{"name":"publication_history","label":"Publication History"}},{"value":"2026-08-24","order":2,"name":"accepted","label":"Accepted","group":{"name":"publication_history","label":"Publication History"}},{"value":"2026-10-18","order":3,"name":"published","label":"Published","group":{"name":"publication_history","label":"Publication History"}}],"article-number":"e71100"}}