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Interspecific complementation-restoration of phenotype in Arabidopsis cuc2cuc3 mutant by sugarcane CUC2 gene

BACKGROUND: In plants, a critical balance between differentiation and proliferation of stem cells at the shoot apical meristem zone is essential for proper growth. The spatiotemporal regulation of some crucial genes dictates the formation of a boundary within and around budding organs. The boundary...

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Autores principales: Aslam, Mohammad, She, Zeyuan, Jakada, Bello Hassan, Fakher, Beenish, Greaves, Joseph G., Yan, Maokai, Chen, Yingzhi, Zheng, Ping, Cheng, Yan, Qin, Yuan
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8783490/
https://www.ncbi.nlm.nih.gov/pubmed/35065620
http://dx.doi.org/10.1186/s12870-022-03440-z
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author Aslam, Mohammad
She, Zeyuan
Jakada, Bello Hassan
Fakher, Beenish
Greaves, Joseph G.
Yan, Maokai
Chen, Yingzhi
Zheng, Ping
Cheng, Yan
Qin, Yuan
author_facet Aslam, Mohammad
She, Zeyuan
Jakada, Bello Hassan
Fakher, Beenish
Greaves, Joseph G.
Yan, Maokai
Chen, Yingzhi
Zheng, Ping
Cheng, Yan
Qin, Yuan
author_sort Aslam, Mohammad
collection PubMed
description BACKGROUND: In plants, a critical balance between differentiation and proliferation of stem cells at the shoot apical meristem zone is essential for proper growth. The spatiotemporal regulation of some crucial genes dictates the formation of a boundary within and around budding organs. The boundary plays a pivotal role in distinguishing one tissue type from another and provides a defined shape to the organs at their developed stage. NAM/CUC subfamily of the NAC transcription factors control the boundary formation during meristematic development. RESULTS: Here, we have identified the CUP-SHAPED COTYLEDON (CUC) genes in sugarcane and named SsCUC2 (for the orthologous gene of CUC1 and CUC2) and SsCUC3. The phylogenetic reconstruction showed that SsCUCs occupy the CUC2 and CUC3 clade together with monocots, whereas eudicot CUC2 and CUC3 settled separately in the different clade. The structural analysis of CUC genes showed that most of the CUC3 genes were accompanied by an intron gain during eudicot divergence. Besides, the study of SsCUCs expression in the RNA-seq obtained during different stages of ovule development revealed that SsCUCs express in developing young tissues, and the expression of SsCUC2 is regulated by miR164. We also demonstrate that SsCUC2 (a monocot) could complement the cuc2cuc3 mutant phenotype of Arabidopsis (eudicot). CONCLUSIONS: This study further supports that CUC2 has diverged in CUC1 and CUC2 during the evolution of monocots and eudicots from ancestral plants. The functional analysis of CUC expression patterns during sugarcane ovule development and ectopic expression of SsCUC2 in Arabidopsis showed that SsCUC2 has a conserved role in boundary formation. Overall, these findings improve our understanding of the functions of sugarcane CUC genes. Our results reveal the crucial functional role of CUC genes in sugarcane. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12870-022-03440-z.
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spelling pubmed-87834902022-01-24 Interspecific complementation-restoration of phenotype in Arabidopsis cuc2cuc3 mutant by sugarcane CUC2 gene Aslam, Mohammad She, Zeyuan Jakada, Bello Hassan Fakher, Beenish Greaves, Joseph G. Yan, Maokai Chen, Yingzhi Zheng, Ping Cheng, Yan Qin, Yuan BMC Plant Biol Research BACKGROUND: In plants, a critical balance between differentiation and proliferation of stem cells at the shoot apical meristem zone is essential for proper growth. The spatiotemporal regulation of some crucial genes dictates the formation of a boundary within and around budding organs. The boundary plays a pivotal role in distinguishing one tissue type from another and provides a defined shape to the organs at their developed stage. NAM/CUC subfamily of the NAC transcription factors control the boundary formation during meristematic development. RESULTS: Here, we have identified the CUP-SHAPED COTYLEDON (CUC) genes in sugarcane and named SsCUC2 (for the orthologous gene of CUC1 and CUC2) and SsCUC3. The phylogenetic reconstruction showed that SsCUCs occupy the CUC2 and CUC3 clade together with monocots, whereas eudicot CUC2 and CUC3 settled separately in the different clade. The structural analysis of CUC genes showed that most of the CUC3 genes were accompanied by an intron gain during eudicot divergence. Besides, the study of SsCUCs expression in the RNA-seq obtained during different stages of ovule development revealed that SsCUCs express in developing young tissues, and the expression of SsCUC2 is regulated by miR164. We also demonstrate that SsCUC2 (a monocot) could complement the cuc2cuc3 mutant phenotype of Arabidopsis (eudicot). CONCLUSIONS: This study further supports that CUC2 has diverged in CUC1 and CUC2 during the evolution of monocots and eudicots from ancestral plants. The functional analysis of CUC expression patterns during sugarcane ovule development and ectopic expression of SsCUC2 in Arabidopsis showed that SsCUC2 has a conserved role in boundary formation. Overall, these findings improve our understanding of the functions of sugarcane CUC genes. Our results reveal the crucial functional role of CUC genes in sugarcane. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12870-022-03440-z. BioMed Central 2022-01-22 /pmc/articles/PMC8783490/ /pubmed/35065620 http://dx.doi.org/10.1186/s12870-022-03440-z Text en © The Author(s) 2022 https://creativecommons.org/licenses/by/4.0/Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/ (https://creativecommons.org/publicdomain/zero/1.0/) ) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
spellingShingle Research
Aslam, Mohammad
She, Zeyuan
Jakada, Bello Hassan
Fakher, Beenish
Greaves, Joseph G.
Yan, Maokai
Chen, Yingzhi
Zheng, Ping
Cheng, Yan
Qin, Yuan
Interspecific complementation-restoration of phenotype in Arabidopsis cuc2cuc3 mutant by sugarcane CUC2 gene
title Interspecific complementation-restoration of phenotype in Arabidopsis cuc2cuc3 mutant by sugarcane CUC2 gene
title_full Interspecific complementation-restoration of phenotype in Arabidopsis cuc2cuc3 mutant by sugarcane CUC2 gene
title_fullStr Interspecific complementation-restoration of phenotype in Arabidopsis cuc2cuc3 mutant by sugarcane CUC2 gene
title_full_unstemmed Interspecific complementation-restoration of phenotype in Arabidopsis cuc2cuc3 mutant by sugarcane CUC2 gene
title_short Interspecific complementation-restoration of phenotype in Arabidopsis cuc2cuc3 mutant by sugarcane CUC2 gene
title_sort interspecific complementation-restoration of phenotype in arabidopsis cuc2cuc3 mutant by sugarcane cuc2 gene
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8783490/
https://www.ncbi.nlm.nih.gov/pubmed/35065620
http://dx.doi.org/10.1186/s12870-022-03440-z
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