{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,6]],"date-time":"2026-10-06T05:56:02Z","timestamp":1791266162275,"version":"4.1.0"},"reference-count":70,"publisher":"Wiley","issue":"5","license":[{"start":{"date-parts":[[2026,10,5]],"date-time":"2026-10-05T00:00:00Z","timestamp":1791158400000},"content-version":"vor","delay-in-days":34,"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\/100012774","name":"Innovationsfonden","doi-asserted-by":"publisher","id":[{"id":"10.13039\/100012774","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                    Ri\/rol transformation by\n                    <jats:styled-content style=\"fixed-case\">\n                      <jats:italic>Rhizobium rhizogenes<\/jats:italic>\n                    <\/jats:styled-content>\n                    is well known to alter plant architecture, including shoot compactness, branching and root development. However, its significance for plant responses to nitrogen limitation remains unclear. Here, we investigated developmental, physiological and hormonal responses of an interspecific\n                    <jats:italic>Kalancho\u00eb laciniata<\/jats:italic>\n                    \u00d7\n                    <jats:styled-content style=\"fixed-case\">\n                      <jats:italic>K. blossfeldiana<\/jats:italic>\n                    <\/jats:styled-content>\n                    hybrid to nitrogen deficiency using complementary pot and hydroponic experiments. Nitrogen deficiency strongly reduced leaf area and total biomass in both wild\u2010type (WT) and rol\u2010transformed (Rol) plants. Nevertheless, rol transformation consistently produced a more compact, highly branched phenotype, with increased leaf number, greater side\u2010shoot formation, higher specific leaf area, lower leaf dry matter content, and, in hydroponics, a striking increase in root mass allocation. Rol plants also maintained higher chlorophyll and carotenoid concentrations than WT and showed altered carbon partitioning, with lower soluble sugars but a higher relative proportion of sucrose. Under nitrogen deficiency, Rol plants maintained positive net photosynthesis and higher electron transport, whereas WT plants showed near\u2010complete suppression of CO\n                    <jats:sub>2<\/jats:sub>\n                    assimilation despite high intercellular CO\n                    <jats:sub>2<\/jats:sub>\n                    concentration, pointing to strong non\u2010stomatal limitation. Rol plants were characterized by lower ABA and PA concentrations, reduced auxin pools and enhanced leaf cytokinin status. Under low N, greater root allocation in Rol plants was not accompanied by reduced overall growth when root expansion was unrestricted, suggesting compensation through higher specific leaf area and maintenance of photosynthetic function. The strong shift towards root investment highlights a potential role of rol transformation in applications where belowground biomass and root development are especially relevant.\n                  <\/jats:p>","DOI":"10.1111\/ppl.71140","type":"journal-article","created":{"date-parts":[[2026,10,6]],"date-time":"2026-10-06T05:34:25Z","timestamp":1791264865000},"update-policy":"https:\/\/doi.org\/10.1002\/crossmark_policy","source":"Crossref","is-referenced-by-count":0,"title":["Rol\u2010Transformed\n                    <scp>\n                      <i>Kalancho\u00eb<\/i>\n                    <\/scp>\n                    Shows Altered Root Allocation and Photosynthetic Responses to Nitrogen Deficiency"],"prefix":"10.1111","volume":"178","author":[{"given":"Alessandro","family":"Esposito","sequence":"first","affiliation":[{"name":"Department of Food Science Aarhus University  Aarhus Denmark"},{"name":"Department of Agricultural, Food and Forest Sciences (SAAF) University of Palermo  Palermo Italy"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Giorgia","family":"Saccardo","sequence":"additional","affiliation":[{"name":"Department of Food Science Aarhus University  Aarhus Denmark"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0009-0006-2649-0820","authenticated-orcid":false,"given":"Yannick Valentin","family":"El Khoury","sequence":"additional","affiliation":[{"name":"Department of Food Science Aarhus University  Aarhus Denmark"},{"name":"Department of Plant and Environmental Sciences University of Copenhagen  Taastrup Denmark"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-3527-1471","authenticated-orcid":false,"given":"Natalia Prieto","family":"Vidal","sequence":"additional","affiliation":[{"name":"Department of Food Science Aarhus University  Aarhus Denmark"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-3074-6810","authenticated-orcid":false,"given":"Ond\u0159ej","family":"Vrobel","sequence":"additional","affiliation":[{"name":"Czech Advanced Technology and Research Institute (CATRIN) Palack\u00fd University Olomouc  Olomouc Czech Republic"},{"name":"Czech Agrifood Research Center, Genetic Resources of Vegetables and Special Crops  Olomouc Czech Republic"},{"name":"Department of Biochemistry, Faculty of Science Palack\u00fd University Olomouc  Olomouc Czech Republic"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-7581-7686","authenticated-orcid":false,"given":"Petr","family":"Tarkowski","sequence":"additional","affiliation":[{"name":"Czech Advanced Technology and Research Institute (CATRIN) Palack\u00fd University Olomouc  Olomouc Czech Republic"},{"name":"Czech Agrifood Research Center, Genetic Resources of Vegetables and Special Crops  Olomouc Czech Republic"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Martina","family":"Paponov","sequence":"additional","affiliation":[{"name":"Queen Genetics\/Knud Jepsen A\/S  Hinnerup Denmark"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jwan","family":"Goreal","sequence":"additional","affiliation":[{"name":"Queen Genetics\/Knud Jepsen A\/S  Hinnerup Denmark"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Kai L\u00f8nne","family":"Nielsen","sequence":"additional","affiliation":[{"name":"Queen Genetics\/Knud Jepsen A\/S  Hinnerup Denmark"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-2138-0722","authenticated-orcid":false,"given":"Ivan A.","family":"Paponov","sequence":"additional","affiliation":[{"name":"Department of Food Science Aarhus University  Aarhus Denmark"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"311","published-online":{"date-parts":[[2026,10,5]]},"reference":[{"key":"e_1_2_10_2_1","doi-asserted-by":"crossref","first-page":"3451","DOI":"10.1007\/s42729-026-03076-0","article-title":"Navigating Patchy Soils: Signaling Networks and Metabolic Responses in Plant Nutrient Foraging","volume":"26","author":"Bhattacharya J.","year":"2026","journal-title":"Journal of Soil Science and Plant Nutrition"},{"key":"e_1_2_10_3_1","doi-asserted-by":"crossref","first-page":"118","DOI":"10.1016\/j.pbi.2016.04.001","article-title":"Orchestration of Carbohydrate Processing for Crassulacean Acid Metabolism","volume":"31","author":"Borland A. 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F.","year":"2020","journal-title":"Plant Cell"},{"key":"e_1_2_10_6_1","doi-asserted-by":"crossref","first-page":"318","DOI":"10.1016\/j.biotechadv.2008.03.001","article-title":"Functions of Rol Genes in Plant Secondary Metabolism","volume":"26","author":"Bulgakov V. P.","year":"2008","journal-title":"Biotechnology Advances"},{"key":"e_1_2_10_7_1","doi-asserted-by":"crossref","first-page":"71","DOI":"10.1080\/00103627509366547","article-title":"Rapid Colorimetric Determination of Nitrate in Plant Tissue by Nitration of Salicylic Acid","volume":"6","author":"Cataldo D. 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R.","year":"2010","journal-title":"Annual Review of Plant Biology"},{"key":"e_1_2_10_11_1","doi-asserted-by":"crossref","first-page":"403","DOI":"10.1007\/s11240-019-01736-x","article-title":"Introgression of Rol Genes From Rhizogenic Agrobacterium Strains Into Escallonia spp","volume":"140","author":"Denaeghel H. E. R.","year":"2020","journal-title":"Plant Cell, Tissue and Organ Culture (PCTOC)"},{"key":"e_1_2_10_12_1","doi-asserted-by":"crossref","first-page":"515","DOI":"10.1007\/s10725-023-01073-2","article-title":"Improved Compact Growth Habit of Viola \u00d7 Wittrockiana Through \n                     Rhizobium rhizogenes\n                   Transformation","volume":"102","author":"Desmet S.","year":"2024","journal-title":"Plant Growth Regulation"},{"key":"e_1_2_10_13_1","doi-asserted-by":"crossref","first-page":"2435","DOI":"10.1007\/s00253-020-10403-7","article-title":"Rhizogenic Agrobacteria as an Innovative Tool for Plant Breeding: Current Achievements and Limitations","volume":"104","author":"Desmet S.","year":"2020","journal-title":"Applied Microbiology and Biotechnology"},{"key":"e_1_2_10_14_1","doi-asserted-by":"crossref","DOI":"10.3389\/fpls.2020.00859","article-title":"Segregation of Rol Genes in Two Generations of \n                     Sinningia speciosa\n                   Engineered Through Wild Type \n                     Rhizobium rhizogenes","volume":"11","author":"Desmet S.","year":"2020","journal-title":"Frontiers in Plant Science"},{"key":"e_1_2_10_15_1","doi-asserted-by":"crossref","first-page":"44","DOI":"10.1104\/pp.114.251827","article-title":"Transgenic Perturbation of the Decarboxylation Phase of Crassulacean Acid Metabolism Alters Physiology and Metabolism but Has Only a Small Effect on Growth","volume":"167","author":"Dever L. V.","year":"2015","journal-title":"Plant Physiology"},{"key":"e_1_2_10_16_1","doi-asserted-by":"crossref","first-page":"211","DOI":"10.1038\/nrm3088","article-title":"Signal Integration in the Control of Shoot Branching","volume":"12","author":"Domagalska M. A.","year":"2011","journal-title":"Nature Reviews. Molecular Cell Biology"},{"key":"e_1_2_10_17_1","doi-asserted-by":"crossref","first-page":"55","DOI":"10.1038\/s41477-020-0590-x","article-title":"Synchronization of Developmental, Molecular and Metabolic Aspects of Source\u2013Sink Interactions","volume":"6","author":"Fernie A. R.","year":"2020","journal-title":"Nature Plants"},{"key":"e_1_2_10_18_1","doi-asserted-by":"crossref","first-page":"769","DOI":"10.1093\/jxb\/ert421","article-title":"It's Time to Make Changes: Modulation of Root System Architecture by Nutrient Signals","volume":"65","author":"Giehl R. F. H.","year":"2014","journal-title":"Journal of Experimental Botany"},{"key":"e_1_2_10_19_1","doi-asserted-by":"crossref","DOI":"10.3389\/fpls.2022.922106","article-title":"Delayed Leaf Senescence by Upregulation of Cytokinin Biosynthesis Specifically in Tomato Roots","volume":"13","author":"Glanz\u2010Idan N.","year":"2022","journal-title":"Frontiers in Plant Science"},{"key":"e_1_2_10_20_1","doi-asserted-by":"crossref","first-page":"1306","DOI":"10.2135\/cropsci1993.0011183X003300060037x","article-title":"Rapid Extraction and Analysis of Nonstructural Carbohydrates in Plant\u2010Tissues","volume":"33","author":"Hendrix D. 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K.","year":"1987"},{"key":"e_1_2_10_29_1","doi-asserted-by":"crossref","first-page":"6621","DOI":"10.1093\/jxb\/erz415","article-title":"CRISPR\/Cas9\u2010Mediated Targeted Mutagenesis for Functional Genomics Research of Crassulacean Acid Metabolism Plants","volume":"70","author":"Liu D.","year":"2019","journal-title":"Journal of Experimental Botany"},{"key":"e_1_2_10_30_1","doi-asserted-by":"crossref","DOI":"10.3389\/fpls.2022.1067498","article-title":"Nutrient Deficiency Effects on Root Architecture and Root\u2010To\u2010Shoot Ratio in Arable Crops","volume":"13","author":"Lopez G.","year":"2023","journal-title":"Frontiers in Plant Science"},{"key":"e_1_2_10_31_1","doi-asserted-by":"crossref","first-page":"70","DOI":"10.1111\/tpj.12448","article-title":"Auxin Biosynthetic Gene TAR2 Is Involved in Low Nitrogen\u2010Mediated Reprogramming of Root Architecture in Arabidopsis","volume":"78","author":"Ma W. Y.","year":"2014","journal-title":"Plant Journal"},{"key":"e_1_2_10_32_1","doi-asserted-by":"crossref","first-page":"10","DOI":"10.1016\/j.plaphy.2021.04.037","article-title":"Agrobacterium rhizogenes\n                   rolB Oncogene: An Intriguing Player for Many Roles","volume":"165","author":"Mauro M. L.","year":"2021","journal-title":"Plant Physiology and Biochemistry"},{"key":"e_1_2_10_33_1","article-title":"Plants Under Stress: Exploring Physiological and Molecular Responses to Nitrogen and Phosphorus Deficiency","volume":"13","author":"Mishra S.","year":"2024","journal-title":"Plants (Basel)"},{"key":"e_1_2_10_34_1","unstructured":"Nielsen K. L.2021.EP3334830 \u2010 Plants Comprising a Low Copy Number of Ri Genes."},{"key":"e_1_2_10_35_1","doi-asserted-by":"crossref","first-page":"729","DOI":"10.1105\/tpc.15.00946","article-title":"Environmental Nitrate Stimulates Abscisic Acid Accumulation in Arabidopsis Root Tips by Releasing It From Inactive Stores","volume":"28","author":"Ondzighi\u2010Assoume C. A.","year":"2016","journal-title":"Plant Cell"},{"key":"e_1_2_10_36_1","first-page":"801","article-title":"CAM Photosynthesis Under Drought Conditions in \n                     Kalanchoe blossfeldiana\n                   Grown With Nitrate or Ammonium as the Sole Nitrogen Source","volume":"29","author":"Ota K.","year":"1988","journal-title":"Plant and Cell Physiology"},{"key":"e_1_2_10_37_1","doi-asserted-by":"crossref","first-page":"1271","DOI":"10.1093\/jxb\/42.10.1271","article-title":"Effects of Different Nitrogen Sources and Concentrations on CAM Photosynthesis in Kalancho\u00eb Blossfeldiana","volume":"42","author":"Ota K.","year":"1991","journal-title":"Journal of Experimental Botany"},{"key":"e_1_2_10_38_1","doi-asserted-by":"crossref","DOI":"10.3390\/plants10030573","article-title":"Nitrogen Deficiency and Synergism Between Continuous Light and Root Ammonium Supply Modulate Distinct but Overlapping Patterns of Phytohormone Composition in Xylem Sap of Tomato Plants","volume":"10","author":"Paponov M.","year":"2021","journal-title":"Plants"},{"key":"e_1_2_10_39_1","doi-asserted-by":"crossref","first-page":"756","DOI":"10.1002\/jpln.200320339","article-title":"Effect of Nitrogen Supply on Leaf Traits Related to Photosynthesis During Grain Filling in Two Maize Genotypes With Different N Efficiency","volume":"166","author":"Paponov I. A.","year":"2003","journal-title":"Journal of Plant Nutrition and Soil Science"},{"key":"e_1_2_10_40_1","doi-asserted-by":"crossref","DOI":"10.3389\/fpls.2023.1174151","article-title":"Heterogeneous Nutrient Supply Modulates Root Exudation and Accumulation of Medicinally Valuable Compounds in \n                     Artemisia Annua\n                   and \n                     Hypericum perforatum","volume":"14","author":"Paponov M.","year":"2023","journal-title":"Frontiers in Plant Science"},{"key":"e_1_2_10_41_1","doi-asserted-by":"crossref","first-page":"467","DOI":"10.1006\/anbo.1999.0935","article-title":"Growth Analysis of Solution Culture\u2010Grown Winter Rye, Wheat and Triticale at Different Relative Rates of Nitrogen Supply","volume":"84","author":"Paponov I. A.","year":"1999","journal-title":"Annals of Botany"},{"key":"e_1_2_10_42_1","doi-asserted-by":"crossref","DOI":"10.3389\/fpls.2020.00586","article-title":"Differential Regulation of Kernel Set and Potential Kernel Weight by Nitrogen Supply and Carbohydrate Availability in Maize Genotypes Contrasting in Nitrogen Use Efficiency","volume":"11","author":"Paponov I. A.","year":"2020","journal-title":"Frontiers in Plant Science"},{"key":"e_1_2_10_43_1","doi-asserted-by":"crossref","first-page":"563","DOI":"10.1006\/anbo.2000.1115","article-title":"Growth and Biomass Allocation, With Varying Nitrogen Availability, of Near\u2010Isogenic Pea Lines With Differing Foliage Structure","volume":"85","author":"Paponov I. A.","year":"2000","journal-title":"Annals of Botany"},{"key":"e_1_2_10_44_1","doi-asserted-by":"crossref","first-page":"904","DOI":"10.1093\/pcp\/pcad128","article-title":"Lipidomic and Metabolomic Analyses Reveal Changes of Lipid and Metabolite Profiles in Rapeseed During Nitrogen Deficiency","volume":"65","author":"Peng Y.","year":"2024","journal-title":"Plant & Cell Physiology"},{"key":"e_1_2_10_45_1","doi-asserted-by":"crossref","DOI":"10.3390\/ijms20184363","article-title":"Exploring the Relationship Between Crassulacean Acid Metabolism (CAM) and Mineral Nutrition With a Special Focus on Nitrogen","volume":"20","author":"Pereira P. N.","year":"2019","journal-title":"International Journal of Molecular Sciences"},{"key":"e_1_2_10_46_1","doi-asserted-by":"crossref","first-page":"361","DOI":"10.1111\/ppl.12578","article-title":"Nitrate Enhancement of CAM Activity in Two Kalancho\u00eb Species Is Associated With Increased Vacuolar Proton Transport Capacity","volume":"160","author":"Pereira P. 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