{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,23]],"date-time":"2026-10-23T19:45:05Z","timestamp":1792784705276,"version":"4.5.0"},"reference-count":59,"publisher":"American Chemical Society (ACS)","issue":"40","license":[{"start":{"date-parts":[[2026,10,1]],"date-time":"2026-10-01T00:00:00Z","timestamp":1790812800000},"content-version":"stm-asf","delay-in-days":0,"URL":"https:\/\/doi.org\/10.15223\/policy-029"},{"start":{"date-parts":[[2026,10,1]],"date-time":"2026-10-01T00:00:00Z","timestamp":1790812800000},"content-version":"stm-asf","delay-in-days":0,"URL":"https:\/\/doi.org\/10.15223\/policy-037"},{"start":{"date-parts":[[2026,10,1]],"date-time":"2026-10-01T00:00:00Z","timestamp":1790812800000},"content-version":"stm-asf","delay-in-days":0,"URL":"https:\/\/doi.org\/10.15223\/policy-045"}],"funder":[{"DOI":"10.13039\/na","name":"Sichuan Science and Technology Program","doi-asserted-by":"publisher","award":["2026NSFSC0102"],"award-info":[{"award-number":["2026NSFSC0102"]}],"id":[{"id":"10.13039\/na","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/na","name":"Interdisciplinary Construction Project of Chengdu University","doi-asserted-by":"publisher","award":["2026XKJC16"],"award-info":[{"award-number":["2026XKJC16"]}],"id":[{"id":"10.13039\/na","id-type":"DOI","asserted-by":"publisher"},{"id":"https:\/\/ror.org\/034z67559","id-type":"ROR","asserted-by":"crossref"}]},{"DOI":"10.13039\/na","name":"China Agriculture Research System","doi-asserted-by":"publisher","award":["CARS-07-B-1"],"award-info":[{"award-number":["CARS-07-B-1"]}],"id":[{"id":"10.13039\/na","id-type":"DOI","asserted-by":"publisher"},{"id":"https:\/\/ror.org\/03p5eky76","id-type":"ROR","asserted-by":"crossref"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":[],"published-print":{"date-parts":[[2026,10,14]]},"abstract":"<jats:title>Abstract<\/jats:title>\n                  <jats:p>Low nitrogen use efficiency caused by irrational nitrogen fertilization restricts Tartary buckwheat (TB) yield improvement. CLE peptides are key signaling molecules regulating plant nitrogen response, yet their functions in TB remain unclear. Herein, 16 FtCLE genes were identified in TB, and all encoding proteins contained conserved bioactive CLE mature peptides. The root-specific and high nitrogen-induced gene, FtCLE7, was screened as the key CLE member by expression analysis. Exogenous synthetic FtCLE7 peptide treatment significantly promoted growth and nitrogen accumulation in TB, and reshaped rhizosphere microbial communities. Transcriptome analysis demonstrated that FtCLE7 peptide changed the expression of genes involved in hormone signaling, phenylpropanoid biosynthesis, transcription regulation, and receptor-like kinases. Additionally, overexpression of FtCLE7 in tobacco verified its positive regulatory role in growth and nitrogen accumulation. This study clarifies the biological function of FtCLE7 in modulating nitrogen accumulation, providing a theoretical basis for breeding nitrogen-efficient TB varieties and developing novel peptide fertilizers.<\/jats:p>","DOI":"10.1021\/acs.jafc.6c07923","type":"journal-article","created":{"date-parts":[[2026,10,2]],"date-time":"2026-10-02T04:01:57Z","timestamp":1790913717000},"page":"31462-31477","source":"Crossref","is-referenced-by-count":0,"title":["Identification\nand Functional Analysis of the\n                    <i>CLAVATA3\/embryo Surrounding Region-Related<\/i>\n                    (\n                    <i>CLE<\/i>\n                    ) Gene Family in Tartary\nBuckwheat Suggests the Promoting Effect\nof FtCLE7 on Growth and Nitrogen Accumulation"],"prefix":"10.1021","volume":"74","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-5573-236X","authenticated-orcid":true,"given":"Changying","family":"Liu","sequence":"first","affiliation":[{"name":"Chengdu University , , , ,","place":["Chengdu, Sichuan, P. R. China, 610106"]},{"name":"Chengdu University , , , ,","place":["Chengdu, Sichuan, P. R. China, 610106"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yaoxuan","family":"Zou","sequence":"additional","affiliation":[{"name":"Chengdu University , , , ,","place":["Chengdu, Sichuan, P. R. China, 610106"]},{"name":"Chengdu University , , , ,","place":["Chengdu, Sichuan, P. R. China, 610106"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jiting","family":"Wang","sequence":"additional","affiliation":[{"name":"Chengdu University , , , ,","place":["Chengdu, Sichuan, P. R. China, 610106"]},{"name":"Chengdu University , , , ,","place":["Chengdu, Sichuan, P. R. China, 610106"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Hanlin","family":"Wang","sequence":"additional","affiliation":[{"name":"Chengdu University , , , ,","place":["Chengdu, Sichuan, P. R. China, 610106"]},{"name":"Chengdu University , , , ,","place":["Chengdu, Sichuan, P. R. China, 610106"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Qi","family":"Wu","sequence":"additional","affiliation":[{"name":"Chengdu University , , , ,","place":["Chengdu, Sichuan, P. R. China, 610106"]},{"name":"Chengdu University , , , ,","place":["Chengdu, Sichuan, P. R. China, 610106"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Sha","family":"Zheng","sequence":"additional","affiliation":[{"name":"Shaanxi University of Science & Technology , , , ,","place":["Xi\u2019an, Shaanxi, P. R. China, 710021"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Xiaoqin","family":"Zheng","sequence":"additional","affiliation":[{"name":"Chengdu University , , , ,","place":["Chengdu, Sichuan, P. R. China, 610106"]},{"name":"Chengdu University , , , ,","place":["Chengdu, Sichuan, P. R. China, 610106"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Maoling","family":"Tan","sequence":"additional","affiliation":[{"name":"Chengdu University , , , ,","place":["Chengdu, Sichuan, P. R. China, 610106"]},{"name":"Chengdu University , , , ,","place":["Chengdu, Sichuan, P. R. China, 610106"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Xi","family":"Wu","sequence":"additional","affiliation":[{"name":"Chengdu University , , , ,","place":["Chengdu, Sichuan, P. R. China, 610106"]},{"name":"Chengdu University , , , ,","place":["Chengdu, Sichuan, P. R. China, 610106"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Daiying","family":"Xu","sequence":"additional","affiliation":[{"name":"Chengdu University , , , ,","place":["Chengdu, Sichuan, P. R. China, 610106"]},{"name":"Chengdu University , , , ,","place":["Chengdu, Sichuan, P. R. China, 610106"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Junjie","family":"Yin","sequence":"additional","affiliation":[{"name":"Chengdu University , , , ,","place":["Chengdu, Sichuan, P. R. China, 610106"]},{"name":"Chengdu University , , , ,","place":["Chengdu, Sichuan, P. R. China, 610106"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yan","family":"Wan","sequence":"additional","affiliation":[{"name":"Chengdu University , , , ,","place":["Chengdu, Sichuan, P. R. China, 610106"]},{"name":"Chengdu University , , , ,","place":["Chengdu, Sichuan, P. R. China, 610106"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Linsen","family":"Mei","sequence":"additional","affiliation":[{"name":"Sichuan Academy of Agricultural Machinery Sciences , , ,","place":["Chengdu, Sichuan, P. R. 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China, 610106"]}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"316","published-online":{"date-parts":[[2026,10,1]]},"reference":[{"key":"2026101408100481800_cit1","doi-asserted-by":"publisher","first-page":"647","DOI":"10.1016\/j.plaphy.2023.02.023","article-title":"Comparative transcriptome and genome analysis unravels the response\nof Tatary buckwheat root to nitrogen deficiency","volume":"196","author":"Liu","year":"2023","journal-title":"Plant Physiol. 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J."},{"key":"2026101408100481800_cit4","doi-asserted-by":"publisher","first-page":"756","DOI":"10.1111\/jipb.13214","article-title":"CRISPR\/Cas9 gene editing and natural\nvariation analysis demonstrate the potential for HvARE1 in improvement of nitrogen use efficiency in barley","volume":"64","author":"Karunarathne","year":"2022","journal-title":"J. Integr. Plant Biol."},{"issue":"6","key":"2026101408100481800_cit5","doi-asserted-by":"publisher","first-page":"806","DOI":"10.1016\/j.molp.2018.03.013","article-title":"MicroRNA528 affects lodging resistance of maize by\nregulating lignin biosynthesis under nitrogen-luxury conditions","volume":"11","author":"Sun","year":"2018","journal-title":"Mol. 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Genet."},{"issue":"1","key":"2026101408100481800_cit17","doi-asserted-by":"publisher","first-page":"399","DOI":"10.1104\/pp.19.01088","article-title":"MtSSPdb:\nThe Medicago truncatula small secreted peptide database","volume":"183","author":"Boschiero","year":"2020","journal-title":"Plant Physiol."},{"key":"2026101408100481800_cit18","doi-asserted-by":"publisher","first-page":"35","DOI":"10.1016\/j.pbi.2016.07.009","article-title":"Long-distance\npeptide signaling essential\nfor nutrient homeostasis in plants","volume":"34","author":"Okamoto","year":"2016","journal-title":"Curr. Opin.\nPlant Biol."},{"key":"2026101408100481800_cit19","doi-asserted-by":"publisher","first-page":"385","DOI":"10.1146\/annurev-arplant-050312-120122","article-title":"Posttranslationally\nmodified small-peptide signals in plants","volume":"65","author":"Matsubayashi","year":"2014","journal-title":"Annu.\nRev. Plant Biol."},{"key":"2026101408100481800_cit20","doi-asserted-by":"publisher","DOI":"10.1199\/tab.0149","article-title":"The function\nof the CLE peptides\nin plant development and plant-microbe interactions","volume":"9","author":"Betsuyaku","year":"2011","journal-title":"Arabidopsis Book"},{"issue":"5","key":"2026101408100481800_cit21","doi-asserted-by":"publisher","first-page":"598","DOI":"10.1016\/j.pbi.2013.08.008","article-title":"Evolutionarily conserved CLE peptide\nsignaling in plant development, symbiosis, and parasitism","volume":"16","author":"Miyawaki","year":"2013","journal-title":"Curr. Opin. Plant Biol."},{"issue":"1","key":"2026101408100481800_cit22","doi-asserted-by":"publisher","DOI":"10.1038\/s41467-023-39074-4","article-title":"PXL1 and SERKs\nact as receptor-coreceptor\ncomplexes for the CLE19 peptide to regulate pollen development","volume":"14","author":"Yu","year":"2023","journal-title":"Nat. Commun."},{"key":"2026101408100481800_cit23","doi-asserted-by":"publisher","DOI":"10.1186\/1471-2229-8-1","article-title":"Bioinformatic analysis of the CLE\nsignaling peptide family","volume":"8","author":"Oelkers","year":"2008","journal-title":"BMC Plant Biol."},{"key":"2026101408100481800_cit24","doi-asserted-by":"publisher","DOI":"10.48130\/ph-0025-0006","article-title":"Plant CLE peptides: Functions, challenges,\nand future prospects","volume":"1","author":"Wang","year":"2025","journal-title":"Plant Hormones"},{"key":"2026101408100481800_cit25","doi-asserted-by":"publisher","first-page":"13869","DOI":"10.1021\/acs.jafc.4c03684","article-title":"Identification\nand application of CLE peptides for drought resistance in Solanaceae crops","volume":"72","author":"Li","year":"2024","journal-title":"J. Agric. 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China:\nLife Sci."},{"issue":"3","key":"2026101408100481800_cit27","doi-asserted-by":"publisher","DOI":"10.1016\/j.xplc.2021.100183","article-title":"NLP1 reciprocally regulates nitrate inhibition of nodulation through\nSUNN-CRA2 signaling in Medicago truncatula","volume":"2","author":"Luo","year":"2021","journal-title":"Plant Commun."},{"issue":"19","key":"2026101408100481800_cit28","doi-asserted-by":"publisher","first-page":"3468","DOI":"10.3390\/plants12193468","article-title":"Nitrogen-activated CLV3\/ESR-related\n4 (CLE4) regulates\nshoot, root, and stolon growth in potato","volume":"12","author":"Gancheva","year":"2023","journal-title":"Plants"},{"issue":"6","key":"2026101408100481800_cit29","doi-asserted-by":"publisher","first-page":"607","DOI":"10.1007\/s11103-016-0472-9","article-title":"CLE peptide signaling and nitrogen\ninteractions in plant root development","volume":"91","author":"Araya","year":"2016","journal-title":"Plant\nMol. 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U.S.A."},{"issue":"1","key":"2026101408100481800_cit31","doi-asserted-by":"publisher","first-page":"222","DOI":"10.1104\/pp.110.153718","article-title":"CLE peptides\ncontrol Medicago truncatula nodulation locally and\nsystemically","volume":"153","author":"Mortier","year":"2010","journal-title":"Plant Physiol."},{"issue":"11","key":"2026101408100481800_cit32","doi-asserted-by":"publisher","first-page":"1456","DOI":"10.3390\/plants9111456","article-title":"Nitrate-induced CLE\npeptide systemically inhibits nodulation in Medicago truncatula","volume":"9","author":"Lebedeva","year":"2020","journal-title":"Plants"},{"issue":"5","key":"2026101408100481800_cit33","doi-asserted-by":"publisher","first-page":"984","DOI":"10.3390\/agronomy11050984","article-title":"CLAVATA3\/EMBRYO SURROUNDING REGION (CLE) gene family in potato (Solanum tuberosum L.): Identification and expression analysis","volume":"11","author":"Gancheva","year":"2021","journal-title":"Agronomy"},{"key":"2026101408100481800_cit34","doi-asserted-by":"publisher","DOI":"10.1016\/j.jfca.2026.108859","article-title":"Influence\nof nitrogen fertilizer and genotype on agronomic traits and nutritional\nquality of Tartary buckwheat (Fagopyrum tataricum Gaertn.)","volume":"150","author":"Liu","year":"2026","journal-title":"J. Food Compos. Anal."},{"key":"2026101408100481800_cit35","doi-asserted-by":"publisher","DOI":"10.1016\/j.tifs.2025.105359","article-title":"Across the\nages: Buckwheat meets era-specific needs","volume":"166","author":"Ding","year":"2025","journal-title":"Trends\nFood Sci. Technol."},{"key":"2026101408100481800_cit36","doi-asserted-by":"publisher","DOI":"10.3389\/fmicb.2023.1240029","article-title":"Interkingdom multi-omics analysis\nreveals the effects of nitrogen application on growth and rhizosphere\nmicrobial community of Tartary buckwheat","volume":"14","author":"Qiu","year":"2023","journal-title":"Front.\nMicrobiol."},{"issue":"3","key":"2026101408100481800_cit37","doi-asserted-by":"publisher","first-page":"276","DOI":"10.1016\/j.jgg.2024.10.007","article-title":"Genetic and\nmolecular mechanisms underlying nitrogen use efficiency\nin maize","volume":"52","author":"Li","year":"2025","journal-title":"J. Genet. 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Plant Sci."},{"issue":"12","key":"2026101408100481800_cit41","doi-asserted-by":"publisher","first-page":"1788","DOI":"10.1093\/mp\/ssu090","article-title":"A novel single-nucleotide mutation\nin a CLAVATA3 gene homolog controls a multilocular\nsilique trait in Brassica rapa L","volume":"7","author":"Fan","year":"2014","journal-title":"Mol. Plant"},{"issue":"11","key":"2026101408100481800_cit42","doi-asserted-by":"publisher","first-page":"2021","DOI":"10.1007\/s12298-025-01670-7","article-title":"Genome-wide identification and expression analysis\nof NRT2 gene family in Tartary buckwheat suggests\nthe potential role of FtNTR2.4 in low nitrogen response","volume":"31","author":"Xu","year":"2025","journal-title":"Physiol. Mol. Biol. Plants"},{"key":"2026101408100481800_cit43","doi-asserted-by":"publisher","DOI":"10.1016\/j.plantsci.2021.111091","article-title":"Dynamic transcriptome\nand co-expression\nanalysis suggest the potential roles of small secreted peptides from\nTartary buckwheat (Fagopyrum tataricum) in low nitrogen\nstress response","volume":"313","author":"Liu","year":"2021","journal-title":"Plant Sci."},{"key":"2026101408100481800_cit44","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1016\/j.plaphy.2021.02.027","article-title":"Nitrate dose-responsive\ntranscriptome analysis identifies transcription factors and small\nsecreted peptides involved in nitrogen response in Tartary buckwheat","volume":"162","author":"Liu","year":"2021","journal-title":"Plant Physiol. Biochem."},{"key":"2026101408100481800_cit45","doi-asserted-by":"publisher","DOI":"10.1016\/j.plantsci.2025.112747","article-title":"Genome-wide identification and functional characterization\nof rapid alkalinization factor 6 as a key peptide regulator of abiotic\nstress tolerance in Tartary buckwheat","volume":"362","author":"Sun","year":"2026","journal-title":"Plant\nSci."},{"issue":"6","key":"2026101408100481800_cit46","doi-asserted-by":"publisher","first-page":"561","DOI":"10.1007\/s11103-020-01059-y","article-title":"CLE2 regulates light-dependent carbohydrate\nmetabolism\nin Arabidopsis shoots","volume":"104","author":"Ma","year":"2020","journal-title":"Plant\nMol. Biol."},{"key":"2026101408100481800_cit47","doi-asserted-by":"publisher","DOI":"10.1038\/ncomms3191","article-title":"Root-derived CLE glycopeptides control nodulation by\ndirect binding to HAR1 receptor kinase","volume":"4","author":"Okamoto","year":"2013","journal-title":"Nat.\nCommun."},{"issue":"5","key":"2026101408100481800_cit48","doi-asserted-by":"publisher","first-page":"909","DOI":"10.1007\/s10265-016-0842-z","article-title":"Expression\nof the CLE-RS3 gene suppresses root nodulation in Lotus japonicus","volume":"129","author":"Nishida","year":"2016","journal-title":"J. Plant Res."},{"issue":"17","key":"2026101408100481800_cit49","doi-asserted-by":"publisher","first-page":"5359","DOI":"10.1093\/jxb\/ert301","article-title":"A CLE-WOX\nsignalling\nmodule regulates root meristem maintenance and vascular tissue development\nin rice","volume":"64","author":"Chu","year":"2013","journal-title":"J. Exp. 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