{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,6,16]],"date-time":"2026-06-16T20:58:18Z","timestamp":1781643498324,"version":"3.54.5"},"reference-count":35,"publisher":"Springer Science and Business Media LLC","issue":"3","license":[{"start":{"date-parts":[[2026,3,23]],"date-time":"2026-03-23T00:00:00Z","timestamp":1774224000000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"},{"start":{"date-parts":[[2026,3,23]],"date-time":"2026-03-23T00:00:00Z","timestamp":1774224000000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"}],"funder":[{"DOI":"10.13039\/501100003983","name":"Iwate University","doi-asserted-by":"crossref","id":[{"id":"10.13039\/501100003983","id-type":"DOI","asserted-by":"crossref"}]}],"content-domain":{"domain":["link.springer.com"],"crossmark-restriction":false},"short-container-title":["J Plant Res"],"published-print":{"date-parts":[[2026,5]]},"abstract":"<jats:title>Abstract<\/jats:title>\n                  <jats:p>\n                    Plants adapted to cool habitats have been suggested to possess Rubisco with a high carboxylation capacity and low CO\n                    <jats:sub>2<\/jats:sub>\n                    affinity, thereby facilitating efficient photosynthesis at low temperatures. Rubisco with a low CO\n                    <jats:sub>2<\/jats:sub>\n                    affinity is believed to be less abundant owing to its concomitant high carboxylation capacity. This study aimed to provide information on these subjects by examining plants with early-spring persistent leaves and alpine plants. In these plants, the turnover rates of Rubisco carboxylation under CO\n                    <jats:sub>2<\/jats:sub>\n                    -saturated conditions (\n                    <jats:italic>k<\/jats:italic>\n                    <jats:sub>cat<\/jats:sub>\n                    <jats:sup>c<\/jats:sup>\n                    ) were low to moderate, similar to those of the control C\n                    <jats:sub>3<\/jats:sub>\n                    crops. The predicted Rubisco CO\n                    <jats:sub>2<\/jats:sub>\n                    affinity, that is, the ratio of Rubisco carboxylase activity under CO\n                    <jats:sub>2<\/jats:sub>\n                    -unsaturated conditions (\n                    <jats:italic>v<\/jats:italic>\n                    <jats:sub>cu<\/jats:sub>\n                    ), measured using reaction mixtures saturated with N\n                    <jats:sub>2<\/jats:sub>\n                    gas containing CO\n                    <jats:sub>2<\/jats:sub>\n                    and O\n                    <jats:sub>2<\/jats:sub>\n                    at present atmospheric levels to\n                    <jats:italic>k<\/jats:italic>\n                    <jats:sub>cat<\/jats:sub>\n                    <jats:sup>c<\/jats:sup>\n                    , tended to be moderate, as observed in the control C\n                    <jats:sub>3<\/jats:sub>\n                    crops. Some of these plants contained Rubisco with a low\n                    <jats:italic>k<\/jats:italic>\n                    <jats:sub>cat<\/jats:sub>\n                    <jats:sup>c<\/jats:sup>\n                    and moderate CO\n                    <jats:sub>2<\/jats:sub>\n                    affinity, although Rubisco with a low\n                    <jats:italic>k<\/jats:italic>\n                    <jats:sub>cat<\/jats:sub>\n                    <jats:sup>c<\/jats:sup>\n                    was reported to exhibit a high CO\n                    <jats:sub>2<\/jats:sub>\n                    affinity. N allocation to Rubisco in these plants was comparable to or slightly lower than that in control C\n                    <jats:sub>3<\/jats:sub>\n                    crops. No significant correlations were observed between N allocation to Rubisco and\n                    <jats:italic>k<\/jats:italic>\n                    <jats:sub>cat<\/jats:sub>\n                    <jats:sup>c<\/jats:sup>\n                    or predicted Rubisco CO\n                    <jats:sub>2<\/jats:sub>\n                    affinity. These results suggest that, for plants with early-spring persistent leaves and alpine plants, Rubisco kinetics is not necessarily advantageous for photosynthesis at low temperatures, and that Rubisco abundance is not necessarily dependent on Rubisco kinetics. The physiological implications of these phenomena are discussed.\n                  <\/jats:p>","DOI":"10.1007\/s10265-026-01701-8","type":"journal-article","created":{"date-parts":[[2026,3,23]],"date-time":"2026-03-23T09:17:24Z","timestamp":1774257444000},"page":"511-518","update-policy":"https:\/\/doi.org\/10.1007\/springer_crossmark_policy","source":"Crossref","is-referenced-by-count":0,"title":["Enzymatic and quantitative properties of Rubisco in C3 herbaceous plants with early-spring persistent leaves and some alpine plants"],"prefix":"10.1007","volume":"139","author":[{"given":"Sakiko","family":"Sugawara","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Kana","family":"Ito","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-8789-5289","authenticated-orcid":false,"given":"Shin-Ichi","family":"Miyazawa","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-2779-6275","authenticated-orcid":false,"given":"Amane","family":"Makino","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-8029-9385","authenticated-orcid":false,"given":"Yuji","family":"Suzuki","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"297","published-online":{"date-parts":[[2026,3,23]]},"reference":[{"key":"1701_CR1","doi-asserted-by":"publisher","first-page":"1036","DOI":"10.1111\/nph.14258","volume":"213","author":"FA Busch","year":"2017","unstructured":"Busch FA, Sage RF (2017) The sensitivity of photosynthesis to O2 and CO2 concentration identifies strong Rubisco control above the thermal optimum. New Phytol 213:1036\u20131051","journal-title":"New Phytol"},{"key":"1701_CR2","doi-asserted-by":"publisher","first-page":"78","DOI":"10.1007\/BF00386231","volume":"149","author":"GD Farquhar","year":"1980","unstructured":"Farquhar GD, von Caemmerer S, Berry JA (1980) A biochemical model of photosynthetic CO2 assimilation in leaves of C3 species. Planta 149:78\u201390","journal-title":"Planta"},{"key":"1701_CR3","doi-asserted-by":"publisher","first-page":"1615","DOI":"10.1093\/jxb\/erm242","volume":"59","author":"U Feller","year":"2008","unstructured":"Feller U, Anders I, Mae T (2008) Rubiscolytics: fate of Rubisco after its enzymatic function in a cell is terminated. J Exp Bot 59:1615\u20131624","journal-title":"J Exp Bot"},{"key":"1701_CR4","doi-asserted-by":"publisher","first-page":"3365","DOI":"10.1021\/acs.biochem.9b00237","volume":"58","author":"AV Flamholz","year":"2019","unstructured":"Flamholz AV, Prywes N, Moran U, Davidi D, Bar-On YM, Oltrogge LM, Alves R, Savage D, Milo R (2019) Revisiting trade-offs between Rubisco kinetic parameters. Biochemistry 58:3365\u20133376","journal-title":"Biochemistry"},{"key":"1701_CR5","doi-asserted-by":"publisher","first-page":"1989","DOI":"10.1111\/pce.12335","volume":"37","author":"J Galm\u00e9s","year":"2014","unstructured":"Galm\u00e9s J, Kapralov MV, Andralojc PJ, Conesa M\u00c0, Keys AF, Parry MAJ, Flexas J (2014) Expanding knowledge of the Rubisco kinetics variability in plant species: environmental and evolutionary trends. Plant Cell Environ 37:1989\u20132001","journal-title":"Plant Cell Environ"},{"key":"1701_CR6","doi-asserted-by":"publisher","first-page":"1421","DOI":"10.1002\/eap.1542","volume":"27","author":"B Ghimire","year":"2017","unstructured":"Ghimire B, Riley WJ, Koven CD, Kattge J, Rogers A, Reich PB, Wright IJ (2017) A global trait-based approach to estimate leaf nitrogen functional allocation from observations. Ecol Appl 27:1421\u20131434","journal-title":"Ecol Appl"},{"key":"1701_CR7","doi-asserted-by":"publisher","first-page":"167","DOI":"10.1016\/0014-5793(78)81085-0","volume":"96","author":"NP Hall","year":"1978","unstructured":"Hall NP, Tolbert NE (1978) A rapid procedure for the isolation of ribulose bisphosphate carboxylase\/oxygenase from spinach leaves. FEBS Lett 96:167\u2013169","journal-title":"FEBS Lett"},{"key":"1701_CR8","doi-asserted-by":"publisher","first-page":"2549","DOI":"10.1104\/pp.16.01846","volume":"171","author":"C Hermida-Carrera","year":"2016","unstructured":"Hermida-Carrera C, Kapralov MV, Galm\u00e9s J (2016) Rubisco catalytic properties and temperature response in crops. Plant Physiol 171:2549\u20132561","journal-title":"Plant Physiol"},{"key":"1701_CR9","doi-asserted-by":"publisher","first-page":"346","DOI":"10.1002\/bimj.200810425","volume":"50","author":"T Hothorn","year":"2008","unstructured":"Hothorn T, Bretz F, Westfall P (2008) Simultaneous inference in general parametric models. Biom J 50:346\u2013363","journal-title":"Biom J"},{"key":"1701_CR10","doi-asserted-by":"publisher","first-page":"299","DOI":"10.1080\/10618600.1996.10474713","volume":"5","author":"R Ihaka","year":"1996","unstructured":"Ihaka R, Gentleman R (1996) R. A Language for data analysis and graphics. J Comput Graph Stat 5:299\u2013314","journal-title":"J Comput Graph Stat"},{"key":"1701_CR11","volume-title":"Encyclopedia of alpine plants in Iwate","author":"M Inawashiro","year":"1991","unstructured":"Inawashiro M, Katayama C (1991) Encyclopedia of alpine plants in Iwate. Iwate Nippo, Morioka. (in Japanese)"},{"key":"1701_CR12","doi-asserted-by":"publisher","first-page":"345","DOI":"10.1626\/pps.12.345","volume":"12","author":"C Ishikawa","year":"2009","unstructured":"Ishikawa C, Hatanaka T, Misoo S, Fukayama H (2009) Screening of high kcat Rubisco among Poaceae for improvement of photosynthetic CO2 assimilation in rice. Plant Prod Sci 12:345\u2013350","journal-title":"Plant Prod Sci"},{"key":"1701_CR13","doi-asserted-by":"publisher","first-page":"255","DOI":"10.1007\/s10265-023-01514-z","volume":"137","author":"K Ito","year":"2024","unstructured":"Ito K, Sugawara S, Kageyama S, Sawaguchi N, Hyotani T, Miyazawa SI, Makino A, Suzuki Y (2024) Equisetum praealtum and E. hyemale have abundant Rubisco with a high catalytic turnover rate and low CO2 affinity. J Plant Res 137:255\u2013264","journal-title":"J Plant Res"},{"key":"1701_CR14","volume-title":"Flowers in Hachimantai","author":"S Kudo","year":"1978","unstructured":"Kudo S (1978) Flowers in Hachimantai. Kagaya Publishing, Akita. (in Japanese)"},{"key":"1701_CR15","doi-asserted-by":"publisher","first-page":"14","DOI":"10.2307\/3546032","volume":"72","author":"G Kudo","year":"1995","unstructured":"Kudo G (1995) Ecological significance of flower heliotropism in the spring ephemeral Adonis Ramosa (Ranunculaceae). Oikos 72:14\u201320","journal-title":"Oikos"},{"key":"1701_CR16","doi-asserted-by":"publisher","first-page":"151","DOI":"10.1034\/j.1399-3054.2001.1130201.x","volume":"113","author":"L Lapointe","year":"2001","unstructured":"Lapointe L (2001) How phenology influences physiology in deciduous forest spring ephemerals. Physiol Plant 113:151\u2013157","journal-title":"Physiol Plant"},{"key":"1701_CR17","unstructured":"Larcher W (2001) \u00d6kophysiologie der Pflanzen 6. Auflage. Eugen Ulmer, Stuttgart"},{"key":"1701_CR18","doi-asserted-by":"publisher","first-page":"226","DOI":"10.1016\/0005-2744(74)90274-5","volume":"358","author":"RM Lilley","year":"1974","unstructured":"Lilley RM, Walker DA (1974) An improved spectrophotometric assay for ribulosebisphosphate carboxylase. Biochim Biophys Acta 358:226\u2013229","journal-title":"Biochim Biophys Acta"},{"key":"1701_CR19","first-page":"179","volume":"28","author":"AW Lowder","year":"2010","unstructured":"Lowder AW, Kraus HT, Blazich FA, Warren SL (2010) Day\/night temperatures influence growth and photosynthesis during containerized production of selected species of Helleborus (Hellebores). J Environ Hort 28:179\u2013186","journal-title":"J Environ Hort"},{"key":"1701_CR20","first-page":"1079","volume":"24","author":"T Mae","year":"1983","unstructured":"Mae T, Makino A, Ohira K (1983) Changes in the amounts of ribulose bisphosphate carboxylase synthesized and degraded during the life span of rice leaf (Oryza sativa L). Plant Cell Physiol 24:1079\u20131086","journal-title":"Plant Cell Physiol"},{"key":"1701_CR21","first-page":"429","volume":"25","author":"A Makino","year":"1984","unstructured":"Makino A, Mae T, Ohira K (1984) Relation between nitrogen and ribulose-l,5-bisphosphate carboxylase in rice leaves from emergence through senescence. Plant Cell Physiol 25:429\u2013437","journal-title":"Plant Cell Physiol"},{"key":"1701_CR22","doi-asserted-by":"publisher","first-page":"57","DOI":"10.1104\/pp.79.1.57","volume":"79","author":"A Makino","year":"1985","unstructured":"Makino A, Mae T, Ohira K (1985) Enzymic properties of ribulose-1,5-bisphosphate carboxylase\/oxygenase purified from rice leaves. Plant Physiol 79:57\u201361","journal-title":"Plant Physiol"},{"key":"1701_CR23","doi-asserted-by":"publisher","first-page":"30","DOI":"10.1007\/BF00394870","volume":"174","author":"A Makino","year":"1988","unstructured":"Makino A, Mae T, Ohira K (1988) Differences between wheat and rice in the enzyme properties of ribulose-1,5-bisphosphate carboxylase\/oxygenase and their relationship to photosynthetic gas exchange. Planta 174:30\u201338","journal-title":"Planta"},{"key":"1701_CR24","doi-asserted-by":"publisher","first-page":"415","DOI":"10.1146\/annurev.pp.35.060184.002215","volume":"35","author":"WL Ogren","year":"1984","unstructured":"Ogren WL (1984) Photorespiration: pathways, regulation, and modification. Annu Rev Plant Physiol 35:415\u2013442","journal-title":"Annu Rev Plant Physiol"},{"key":"1701_CR25","doi-asserted-by":"publisher","first-page":"1447","DOI":"10.1111\/nph.14496","volume":"214","author":"Y Onoda","year":"2017","unstructured":"Onoda Y, Wright IJ, Evans JR, Hikosaka K, Kitajima K, Niinemets \u00dc, Poorter H, Tosens T, Westoby M (2017) Physiological and structural tradeoffs underlying the leaf economics spectrum. New Phytol 214:1447\u20131463","journal-title":"New Phytol"},{"key":"1701_CR26","first-page":"707","volume":"172","author":"DJ Orr","year":"2016","unstructured":"Orr DJ, Alc\u00e2ntara A, Kapralov MV, Andralojc PJ, Carmo-Silva E, Parry MAJ (2016) Surveying Rubisco diversity and temperature response to improve crop photosynthetic efficiency. Plant Physiol 172:707\u2013717","journal-title":"Plant Physiol"},{"key":"1701_CR27","doi-asserted-by":"publisher","first-page":"398","DOI":"10.1111\/j.1399-3054.1997.tb01014.x","volume":"101","author":"CD Reid","year":"1997","unstructured":"Reid CD, Tissue DT, Fiscus EL, Strain BR (1997) Comparison of spectrophotometric and radioisotopic methods for the assay of Rubisco in ozone-treated plants. Physiol Plant 101:398\u2013404","journal-title":"Physiol Plant"},{"key":"1701_CR28","doi-asserted-by":"publisher","first-page":"609","DOI":"10.1093\/jexbot\/53.369.609","volume":"53","author":"RF Sage","year":"2002","unstructured":"Sage RF (2002) Variation in the kcat of Rubisco in C3 and C4 plants and some implications for photosynthetic performance at high and low temperature. J Exp Bot 53:609\u2013620","journal-title":"J Exp Bot"},{"key":"1701_CR29","doi-asserted-by":"publisher","first-page":"1086","DOI":"10.1111\/j.1365-3040.2007.01682.x","volume":"30","author":"RF Sage","year":"2007","unstructured":"Sage RF, Kubien DS (2007) The temperature response of C3 and C4 photosynthesis. Plant Cell Environ 30:1086\u20131106","journal-title":"Plant Cell Environ"},{"key":"1701_CR31","doi-asserted-by":"publisher","first-page":"100119","DOI":"10.1016\/j.envc.2021.100119","volume":"4","author":"MR Seyedabadi","year":"2021","unstructured":"Seyedabadi MR, Eicker U, Karimi S (2021) Plant selection for green roofs and their impact on carbon sequestration and the building carbon footprint. Environ Chall 4:100119","journal-title":"Environ Chall"},{"key":"1701_CR30","doi-asserted-by":"publisher","first-page":"53","DOI":"10.1007\/BF02861058","volume":"51","author":"TD Sharkey","year":"1985","unstructured":"Sharkey TD (1985) Photosynthesis in intact leaves of C3 plants: physics, physiology and rate limitations. Bot Rev 51:53\u2013105","journal-title":"Bot Rev"},{"key":"1701_CR34","first-page":"55","volume":"59","author":"Y Suda","year":"1999","unstructured":"Suda Y, Hasegawa W (1999) Plant phenology in Morioka City. V. Annu rep fac edu. Univ Iwate 59:55\u201382 (in Japanese)","journal-title":"Univ Iwate"},{"key":"1701_CR33","first-page":"179","volume":"56","author":"Y Suda","year":"1996","unstructured":"Suda Y, Shirasawa S (1996) Flower calendar Yahaba town, Shiwa district, Iwate Prefecture. II Annu Rep Fac Edu Univ Iwate 56:179\u2013204 (in Japanese)","journal-title":"II Annu Rep Fac Edu Univ Iwate"},{"key":"1701_CR32","doi-asserted-by":"publisher","first-page":"315","DOI":"10.1007\/s10265-024-01606-4","volume":"138","author":"S Sugawara","year":"2025","unstructured":"Sugawara S, Ito K, Miyazawa S, Makino A, Suzuki Y (2025) Enzymatic and quantitative properties of Rubisco in some conifers and lycopods. J Plant Res 138:315\u2013321","journal-title":"J Plant Res"},{"key":"1701_CR35","doi-asserted-by":"publisher","first-page":"55","DOI":"10.1093\/pcp\/pcac139","volume":"64","author":"Y Suzuki","year":"2023","unstructured":"Suzuki Y, Ohsaki K, Takahashi Y, Wada S, Miyake C, Makino A (2023) Behavior of photosystems II and I is modulated depending on N partitioning to Rubisco in mature leaves acclimated to low N levels and senescent leaves in rice. Plant Cell Physiol 64:55\u201363","journal-title":"Plant Cell Physiol"}],"container-title":["Journal of Plant Research"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/link.springer.com\/content\/pdf\/10.1007\/s10265-026-01701-8.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/link.springer.com\/article\/10.1007\/s10265-026-01701-8","content-type":"text\/html","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/link.springer.com\/content\/pdf\/10.1007\/s10265-026-01701-8.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2026,6,16]],"date-time":"2026-06-16T20:41:45Z","timestamp":1781642505000},"score":1,"resource":{"primary":{"URL":"https:\/\/link.springer.com\/10.1007\/s10265-026-01701-8"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2026,3,23]]},"references-count":35,"journal-issue":{"issue":"3","published-print":{"date-parts":[[2026,5]]}},"alternative-id":["1701"],"URL":"https:\/\/doi.org\/10.1007\/s10265-026-01701-8","relation":{},"ISSN":["0918-9440","1618-0860"],"issn-type":[{"value":"0918-9440","type":"print"},{"value":"1618-0860","type":"electronic"}],"subject":[],"published":{"date-parts":[[2026,3,23]]},"assertion":[{"value":"27 October 2025","order":1,"name":"received","label":"Received","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"10 February 2026","order":2,"name":"accepted","label":"Accepted","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"23 March 2026","order":3,"name":"first_online","label":"First Online","group":{"name":"ArticleHistory","label":"Article History"}},{"order":1,"name":"Ethics","group":{"name":"EthicsHeading","label":"Declarations"}},{"value":"The authors declare no competing interests relevant to the content of this article.","order":2,"name":"Ethics","group":{"name":"EthicsHeading","label":"Conflict of interest"}}]}}