Genome-wide mining of wheat B-BOX zinc finger (BBX) gene family provides new insights into light stress responses
Shuhui Chen A , Wenqiang Jiang A , Junliang Yin A , Shuping Wang A , Zhengwu Fang A , Dongfang Ma
A C and Derong Gao A B C
+ Author Affiliations
- Author Affiliations
A Hubei Collaborative Innovation Center for Grain Industry, Engineering Research Center of Ecology and Agricultural Use of Wetland (Ministry of Education), College of Agriculture, Yangtze University, Jingzhou 434000, Hubei, PR China.
B Lixiahe Regional Institute of Agricultural Sciences of Jiangsu, Key Laboratory of Wheat Biology and Genetic Breeding in the Middle and Lower Yangtze River (Ministry of Agriculture), Yangzhou 225007, Jiangsu, PR China.
C Corresponding authors. Emails: madf@yangtzeu.edu.cn; gdr@wheat.org.cn
Crop and Pasture Science 72(1) 17-37 https://doi.org/10.1071/CP20342
Submitted: 3 September 2020 Accepted: 26 October 2020 Published: 8 January 2021
Abstract
The B-BOX (BBX) proteins are an important class of zinc-finger transcription factors involved in the regulation of plant growth and development, and have been identified in many plant species. However, there is no systematic study of common wheat (Triticum aestivum L.) BBX genes. Through comprehensive bioinformatics analysis, we identified and characterised 96 BBX genes from wheat, and provided the genes with a unified nomenclature. We describe the chromosomal location, gene structure, conserved domains, phylogenetic relationships and promoter cis-elements of TaBBX family members. The expression patterns under different conditions, especially under different hormones and light–dark conditions, were studied in detail. According to the diversity of conserved domains, we divided TaBBX proteins into five subfamilies. Gene-duplication analysis showed that duplication of chromosome segments was the main reason for the expansion of the TaBBX gene family. Detecting the expression profiles of six TaBBX genes in different tissues by quantitative real-time PCR, we found that the six genes are regulated under light–dark treatment, and that some TaBBX genes (TaBBX2.11, TaBBX2.13, TaBBX2.15 and TaBBX3.10) are strongly induced by the plant hormones abscisic acid, indole-3-acetic acid and salicylic acid. Our analysis of wheat BBX genes at the genomic level will provide a solid foundation for further identifying the functions of specific genes in light stress responses.
Keywords: ABA, abiotic stress, breeding strategies, crop improvement, IAA, plant growth regulators, wheat.
References
Artimo P, Jonnalagedda M, Arnold K, Baratin D, Csardi G, De Castro E, Stockinger H (2012) ExPASy: SIB bioinformatics resource portal. Nucleic Acids Research 40, 597–603.| ExPASy: SIB bioinformatics resource portal.Crossref | GoogleScholarGoogle Scholar |
Bailey TL, Johnson JR, Grant CE, Noble WS (2015) The MEME Suite. Nucleic Acids Research 43, 39–49.
| The MEME Suite.Crossref | GoogleScholarGoogle Scholar |
Cannon SB, Mitra A, Baumgarten A, Young ND, May G (2004) The roles of segmental and tandem gene duplication in the evolution of large gene families in Arabidopsis thaliana. BMC Plant Biology 4, 10
| The roles of segmental and tandem gene duplication in the evolution of large gene families in Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar | 15171794PubMed |
Cao YP, Han YH, Meng DD, Li DH, Jiao CY, Jin Q, Lin Y, Cai YP (2017) B-BOX genes: genome-wide identification, evolution and their contribution to pollen growth in pear (Pyrus bretschneideri Rehd). BMC Plant Biology 17, 156
| B-BOX genes: genome-wide identification, evolution and their contribution to pollen growth in pear (Pyrus bretschneideri Rehd).Crossref | GoogleScholarGoogle Scholar |
Casal JJ, Fankhauser C, Coupland G, Blazquez MA (2004) Signalling for developmental plasticity. Trends in Plant Science 9, 309–314.
| Signalling for developmental plasticity.Crossref | GoogleScholarGoogle Scholar | 15165563PubMed |
Chang CJ, Maloof JN, Wu S (2011) COP1-mediated degradation of BBX22/LZF1 optimizes seedling development in Arabidopsis. Plant Physiology 156, 228–239.
| COP1-mediated degradation of BBX22/LZF1 optimizes seedling development in Arabidopsis.Crossref | GoogleScholarGoogle Scholar |
Chen CJ, Xia R, Chen H, He YH (2020) TBtools – an integrative toolkit developed for interactive analyses of big biological data. Molecular Plant 13, 1194–1202.
| TBtools – an integrative toolkit developed for interactive analyses of big biological data.Crossref | GoogleScholarGoogle Scholar |
Chou KC, Shen HB (2010) Plant-mPLoc: a top-down strategy to augment the power for predicting plant protein subcellular localization. PLoS One 5, e11335
| Plant-mPLoc: a top-down strategy to augment the power for predicting plant protein subcellular localization.Crossref | GoogleScholarGoogle Scholar | 20596258PubMed |
Chu ZN, Wang X, Li Y, Yu HY, Li J, Lu YE, Ouyang B (2016) Genomic organization, phylogenetic and expression analysis of the B-BOX gene family in tomato. Frontiers in Plant Science 7, 1552
| Genomic organization, phylogenetic and expression analysis of the B-BOX gene family in tomato.Crossref | GoogleScholarGoogle Scholar |
Crocco CD, Botto JF (2013) BBX proteins in green plants: Insights into their evolution, structure, feature and functional diversification. Gene 531, 44–52.
| BBX proteins in green plants: Insights into their evolution, structure, feature and functional diversification.Crossref | GoogleScholarGoogle Scholar | 23988504PubMed |
Crocco CD, Holm M, Yanovsky MJ, Botto JF (2011) Function of B-BOX under shade. Plant Signaling & Behavior 6, 101–104.
| Function of B-BOX under shade.Crossref | GoogleScholarGoogle Scholar |
Crooks GE, Hon G, Chandonia JM, Brenner SE (2004) WebLogo: a sequence logo generator. Genome Research 14, 1188–1190.
| WebLogo: a sequence logo generator.Crossref | GoogleScholarGoogle Scholar | 15173120PubMed |
Ding L, Wang S, Song ZT, Jiang YP, Han JJ, Lu SJ, Lin L, Liu JX (2018) Two B-Box domain proteins, BBX18 and BBX23, interact with ELF3 and regulate thermomorphogenesis in Arabidopsis. Cell Reports 25, 1718–1728.
| Two B-Box domain proteins, BBX18 and BBX23, interact with ELF3 and regulate thermomorphogenesis in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 30428343PubMed |
Fang ZW, Sun C, Lu T, Xu Z, Huang WD, Ma DF, Yin JL (2019) Molecular mapping of stripe rust resistance gene YrH922 in a derivative of wheat (Triticum aestivum)–Psathyrostachys huashanica. Crop & Pasture Science 70, 939–945.
| Molecular mapping of stripe rust resistance gene YrH922 in a derivative of wheat (Triticum aestivum)–Psathyrostachys huashanica.Crossref | GoogleScholarGoogle Scholar |
Fang ZW, Jiang WQ, He YQ, Ma DF, Liu YK, Wang SP, Zhang XY, Yin JL (2020) Genome-wide identification, structure characterization, and expression profiling of Dof transcription factor gene family in wheat (Triticum aestivum L.). Agronomy 10, 294
| Genome-wide identification, structure characterization, and expression profiling of Dof transcription factor gene family in wheat (Triticum aestivum L.).Crossref | GoogleScholarGoogle Scholar |
Fatima A, Khan MJ, Awan HM, Akhtar MN, Bibi N, Sughra K, Khan MR, Ahmad R, Ibrahim M, Hussain J, Sadiq I (2020) Genome-wide identification and expression analysis of SnRK2 gene family in mungbean (Vigna radiata) in response to drought stress. Crop & Pasture Science 71, 469–476.
| Genome-wide identification and expression analysis of SnRK2 gene family in mungbean (Vigna radiata) in response to drought stress.Crossref | GoogleScholarGoogle Scholar |
Gangappa SN, Botto JF (2014) The BBX family of plant transcription factors. Trends in Plant Science 19, 460–470.
| The BBX family of plant transcription factors.Crossref | GoogleScholarGoogle Scholar | 24582145PubMed |
Gendron JM, Pruneda-Paz JL, Doherty CJ, Gross AM, Kang SE, Kay SA (2012) Arabidopsis circadian clock protein, TOC1, is a DNA-binding transcription factor. Proceedings of the National Academy of Sciences of the United States of America 109, 3167–3172.
| Arabidopsis circadian clock protein, TOC1, is a DNA-binding transcription factor.Crossref | GoogleScholarGoogle Scholar | 22315425PubMed |
González-Schain N, Diazmendoza M, Żurczak M, Suarezlopez P (2012) Potato CONSTANS is involved in photoperiodic tuberization in a graft-transmissible manner. The Plant Journal 70, 678–690.
| Potato CONSTANS is involved in photoperiodic tuberization in a graft-transmissible manner.Crossref | GoogleScholarGoogle Scholar | 22260207PubMed |
Griffiths S, Dunford RP, Coupland G, Laurie DA (2003) The evolution of CONSTANS-like gene families in barley, rice, and Arabidopsis. Plant Physiology 131, 1855–1867.
| The evolution of CONSTANS-like gene families in barley, rice, and Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 12692345PubMed |
He YQ, Huang WD, Yang L, Li YT, Lu C, Zhu YX, Ma DF, Yin JL (2020) Genome‐wide analysis of ethylene‐insensitive3 (EIN3/EIL) in Triticum aestivum. Crop Science 60, 2019–2037.
Hu B, Jin J, Guo A, Zhang H, Luo J, Gao G (2015a) GSDS 2.0: an upgraded gene feature visualization server. Bioinformatics 31, 1296–1297.
| GSDS 2.0: an upgraded gene feature visualization server.Crossref | GoogleScholarGoogle Scholar | 25504850PubMed |
Hu W, Hou XW, Huang C, Yan Y, Tie WW, Ding ZH, Wei YX, Liu JH, Miao HX, Lu ZW, Li MY, Xu BY, Jin ZQ (2015b) Genome-wide identification and expression analyses of Aquaporin gene family during development and abiotic stress in banana. International Journal of Molecular Sciences 16, 19728–19751.
| Genome-wide identification and expression analyses of Aquaporin gene family during development and abiotic stress in banana.Crossref | GoogleScholarGoogle Scholar | 26307965PubMed |
Huang JY, Zhao XB, Weng XY, Wang L, Xie WB (2012) The rice B-Box zinc finger gene family: genomic identification, characterization, expression profiling and diurnal analysis. PLoS One 7, e48242
| The rice B-Box zinc finger gene family: genomic identification, characterization, expression profiling and diurnal analysis.Crossref | GoogleScholarGoogle Scholar | 22761690PubMed |
Jiang WJ, Yang LY, He Yq, Zhang HZ, Li WL, Chen HC, Ma DF, Yin JY (2019) Genome-wide identification and transcriptional expression analysis of superoxide dismutase (SOD) family in wheat (Triticum aestivum). PeerJ 7, e8062
| Genome-wide identification and transcriptional expression analysis of superoxide dismutase (SOD) family in wheat (Triticum aestivum).Crossref | GoogleScholarGoogle Scholar |
Jiang WQ, Geng YP, Liu YK, Chen SH, Cao SH, Li W, Chen HG, Ma DF, Yin JL (2020a) Genome-wide identification and characterization of SRO gene family in wheat: molecular evolution and expression profiles during different stresses. Plant Physiology and Biochemistry 154, 590–611.
| Genome-wide identification and characterization of SRO gene family in wheat: molecular evolution and expression profiles during different stresses.Crossref | GoogleScholarGoogle Scholar |
Jiang WQ, Yin JL, Zhang HT, He YQ, Shuai SM, Chen SH, Cao SL, Li W, Ma DF, Chen HG (2020b) Genome-wide identification, characterization analysis and expression profiling of auxin-responsive GH3 family genes in wheat (Triticum aestivum L.). Molecular Biology Reports 47, 3885–3907.
| Genome-wide identification, characterization analysis and expression profiling of auxin-responsive GH3 family genes in wheat (Triticum aestivum L.).Crossref | GoogleScholarGoogle Scholar |
Khanna R, Kronmiller B, Maszle DR, Coupland G, Holm M, Mizuno T, Wu S (2009) The Arabidopsis B-Box zinc finger family. The Plant Cell 21, 3416–3420.
| The Arabidopsis B-Box zinc finger family.Crossref | GoogleScholarGoogle Scholar | 19920209PubMed |
Kobayashi F, Takumi S, Handa H (2010) Identification of quantitative trait loci for ABA responsiveness at the seedling stage associated with ABA-regulated gene expression in common wheat. Theoretical and Applied Genetics 121, 629–641.
| Identification of quantitative trait loci for ABA responsiveness at the seedling stage associated with ABA-regulated gene expression in common wheat.Crossref | GoogleScholarGoogle Scholar | 20401645PubMed |
Kumagai T, Ito S, Nakamichi N, Niwa Y, Murakami M, Yamashino T, Mizuno T (2008) The common function of a novel subfamily of B-Box zinc finger proteins with reference to circadian-associated events in Arabidopsis thaliana. Bioscience, Biotechnology, and Biochemistry 72, 1539–1549.
| The common function of a novel subfamily of B-Box zinc finger proteins with reference to circadian-associated events in Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar | 18540109PubMed |
Kumar S, Stecher G, Tamura K (2016) MEGA7: Molecular Evolutionary Genetics Analysis version 7.0 for bigger datasets. Molecular Biology and Evolution 33, 1870–1874.
| MEGA7: Molecular Evolutionary Genetics Analysis version 7.0 for bigger datasets.Crossref | GoogleScholarGoogle Scholar | 27004904PubMed |
Law C, Sutka J, Worland A (1978) A genetic study of day-length response in wheat. Heredity 41, 185–191.
| A genetic study of day-length response in wheat.Crossref | GoogleScholarGoogle Scholar |
Ledger S, Strayer CA, Ashton F, Kay SA, Putterill J (2001) Analysis of the function of two circadian-regulated CONSTANS-LIKE genes. The Plant Journal 26, 15–22.
| Analysis of the function of two circadian-regulated CONSTANS-LIKE genes.Crossref | GoogleScholarGoogle Scholar | 11359606PubMed |
Lee Y, Jeong D, Lee D, Yi J, Ryu C, Kim SL, Jeor HJ, Choi SC, Jin P, Yang JG, Cho L, Choi H, An G (2010) OsCOL4 is a constitutive flowering repressor upstream of Ehd1 and downstream of OsphyB. The Plant Journal 63, 18–30.
| OsCOL4 is a constitutive flowering repressor upstream of Ehd1 and downstream of OsphyB.Crossref | GoogleScholarGoogle Scholar | 20409004PubMed |
Lescot M, Dehais P, Thijs G, Marchal K, Morea Y, De Peer YV, Rombauts S (2002) PlantCARE, a database of plant cis-acting regulatory elements and a portal to tools for in silico analysis of promoter sequences. Nucleic Acids Research 30, 325–327.
| PlantCARE, a database of plant cis-acting regulatory elements and a portal to tools for in silico analysis of promoter sequences.Crossref | GoogleScholarGoogle Scholar | 11752327PubMed |
Lin FL, Jiang Y, Li J, Yan T, Fan LM, Liang JS, Chen ZJ, Xu DQ, Deng XW (2018) B-BOX DOMAIN PROTEIN28 negatively regulates photomorphogenesis by repressing the activity of transcription factor HY5 and undergoes COP1-mediated degradation. The Plant Cell 30, 2006–2019.
| B-BOX DOMAIN PROTEIN28 negatively regulates photomorphogenesis by repressing the activity of transcription factor HY5 and undergoes COP1-mediated degradation.Crossref | GoogleScholarGoogle Scholar |
Magadum S, Banerjee U, Murugan P, Gangapur D, Ravikesavan R (2013) Gene duplication as a major force in evolution. Journal of Genetics 92, 155–161.
| Gene duplication as a major force in evolution.Crossref | GoogleScholarGoogle Scholar | 23640422PubMed |
Massiah MA, Matts J, Short KM, Simmons B, Singireddy S, Yi Z, Cox TC (2007) Solution structure of the MID1 B-box2 CHC(D/C) C2H2 zinc-binding domain: insights into an evolutionarily conserved RING fold. Journal of Molecular Biology 369, 1–10.
| Solution structure of the MID1 B-box2 CHC(D/C) C2H2 zinc-binding domain: insights into an evolutionarily conserved RING fold.Crossref | GoogleScholarGoogle Scholar | 17428496PubMed |
Mohler V, Lukman R, Ortiz-Islas S, William M, Worland AJ, Beem J, Wenzel G (2004) Genetic and physical mapping of photoperiod insensitive gene Ppd-B1 in common wheat. Euphytica 138, 33–40.
| Genetic and physical mapping of photoperiod insensitive gene Ppd-B1 in common wheat.Crossref | GoogleScholarGoogle Scholar |
Paolacci AR, Tanzarella OA, Porceddu E, Ciaffi M (2009) Identification and validation of reference genes for quantitative RT-PCR normalization in wheat. BMC Molecular Biology 10, 11
| Identification and validation of reference genes for quantitative RT-PCR normalization in wheat.Crossref | GoogleScholarGoogle Scholar | 19232096PubMed |
Peng XJ, Zhao Y, Cao JG, Zhang W, Jiang HY, Li XY, Ma Q, Zhu SW, Cheng BJ (2012) CCCH-type zinc finger family in maize: genome-wide identification, classification and expression profiling under abscisic acid and drought treatments. PLoS One 7, e40120
| CCCH-type zinc finger family in maize: genome-wide identification, classification and expression profiling under abscisic acid and drought treatments.Crossref | GoogleScholarGoogle Scholar |
Peng FY, Hu ZQ, Yang RC (2015) Genome-wide comparative analysis of flowering-related genes in Arabidopsis, wheat, and barley. International Journal of Plant Genomic 2015, 874361
| Genome-wide comparative analysis of flowering-related genes in Arabidopsis, wheat, and barley.Crossref | GoogleScholarGoogle Scholar |
Peterson GI, Masel J (2009) Quantitative prediction of molecular clock and Ka/Ks at short timescales. Molecular Biology and Evolution 26, 2595–2603.
| Quantitative prediction of molecular clock and Ka/Ks at short timescales.Crossref | GoogleScholarGoogle Scholar | 19661199PubMed |
Quraishi UM, Abrouk M, Murat F, Pont C, Foucrier S, Desmaizieres G, Salse J (2011) Cross-genome map based dissection of a nitrogen use efficiency ortho-metaQTL in bread wheat unravels concerted cereal genome evolution. The Plant Journal 65, 745–756.
| Cross-genome map based dissection of a nitrogen use efficiency ortho-metaQTL in bread wheat unravels concerted cereal genome evolution.Crossref | GoogleScholarGoogle Scholar | 21251102PubMed |
Ramirezgonzalez RH, Borrill P, Lang D, Harrington SA, Brinton J, Venturini L, Uauy C (2018) The transcriptional landscape of polyploid wheat. Science 361, 6403
| The transcriptional landscape of polyploid wheat.Crossref | GoogleScholarGoogle Scholar |
Robson F, Costa M, Hepworth SR, Vizir I, Pineiro M, Reeves PH, Coupland G (2001) Functional importance of conserved domains in the flowering‐time gene CONSTANS demonstrated by analysis of mutant alleles and transgenic plants. The Plant Journal 28, 619–631.
| Functional importance of conserved domains in the flowering‐time gene CONSTANS demonstrated by analysis of mutant alleles and transgenic plants.Crossref | GoogleScholarGoogle Scholar | 11851908PubMed |
Santner A, Calderonvillalobos LI, Estelle M (2009) Plant hormones are versatile chemical regulators of plant growth. Nature Chemical Biology 5, 301–307.
| Plant hormones are versatile chemical regulators of plant growth.Crossref | GoogleScholarGoogle Scholar | 19377456PubMed |
Seki M, Chono M, Nishimura T, Sato M, Yoshimura Y, Matsunaka H, Kojima H (2013) Distribution of photoperiod-insensitive allele Ppd-A1a and its effect on heading time in Japanese wheat cultivars. Breeding Science 63, 309–316.
| Distribution of photoperiod-insensitive allele Ppd-A1a and its effect on heading time in Japanese wheat cultivars.Crossref | GoogleScholarGoogle Scholar | 24273426PubMed |
Shalmani A, Fan S, Jia P, Li G, Muhammad I, Li Y, Sharif R, Dong F, Zuo XY, Li K, Chen KM, Han MY (2018) Genome identification of B-BOX gene family members in seven Rosaceae species and their expression analysis in response to flower induction in Malus domestica. Molecules 23, 1763
| Genome identification of B-BOX gene family members in seven Rosaceae species and their expression analysis in response to flower induction in Malus domestica.Crossref | GoogleScholarGoogle Scholar |
Shalmani A, Jing XQ, Shi Y, Muhammad I, Zhou MR, Wei XY, Chen QQ, Li WQ, Liu WT, Chen KM (2019) Characterization of B-BOX gene family and their expression profiles under hormonal, abiotic and metal stresses in Poaceae plants. BMC Genomics 20, 27
| Characterization of B-BOX gene family and their expression profiles under hormonal, abiotic and metal stresses in Poaceae plants.Crossref | GoogleScholarGoogle Scholar | 30626335PubMed |
Soitamo AJ, Piippo M, Allahverdiyeva Y, Battchikova N, Aro E (2008) Light has a specific role in modulating Arabidopsis gene expression at low temperature. BMC Plant Biology 8, 13
| Light has a specific role in modulating Arabidopsis gene expression at low temperature.Crossref | GoogleScholarGoogle Scholar | 18230142PubMed |
Song XY (2015) QTL mapping analysis for traits associated with drought tolerance in wheat seedling. Master’s thesis, Qingdao Agricultural University, Shandong, China.
Song JH, Ma DF, Yin JL, Yang L, He YQ, Zhu ZW, Tong HW, Chen L, Zhu G, Liu YK, Gao C (2019) Genome-wide characterization and expression profiling of Squamosa Promoter Binding Protein-like (SBP) transcription factors in wheat (Triticum aestivum L.). Agronomy 9, 527
| Genome-wide characterization and expression profiling of Squamosa Promoter Binding Protein-like (SBP) transcription factors in wheat (Triticum aestivum L.).Crossref | GoogleScholarGoogle Scholar |
Song ZQ, Bian YT, Liu JJ, Sun YT, Xu DQ (2020) B‐box proteins: pivotal players in light‐mediated development in plants. Journal of Integrative Plant Biology 62, 1293–1309.
| B‐box proteins: pivotal players in light‐mediated development in plants.Crossref | GoogleScholarGoogle Scholar |
Talar U, Kielbowiczmatuk A, Czarnecka J, Rorat T (2017) Genome-wide survey of B-box proteins in potato (Solanum tuberosum): identification, characterization and expression patterns during diurnal cycle, etiolation and de-etiolation. PLoS One 12, e0177471
| Genome-wide survey of B-box proteins in potato (Solanum tuberosum): identification, characterization and expression patterns during diurnal cycle, etiolation and de-etiolation.Crossref | GoogleScholarGoogle Scholar | 28552939PubMed |
Vatansever R, Filiz E, Eroglu S (2017) Genome-wide exploration of metal tolerance protein (MTP) genes in common wheat (Triticum aestivum): insights into metal homeostasis and biofortification. Biometals 30, 217–235.
| Genome-wide exploration of metal tolerance protein (MTP) genes in common wheat (Triticum aestivum): insights into metal homeostasis and biofortification.Crossref | GoogleScholarGoogle Scholar | 28150142PubMed |
Wang QM, Tu XJ, Deng KQ, Zeng JX, Zhao XY, Tang DY, Liu XM (2009) A defect in zinc finger protein bouble B-box 1a (DBB1a) causes abnormal floral development in Arabidopsis. Journal of Plant Biology 52, 543–549.
| A defect in zinc finger protein bouble B-box 1a (DBB1a) causes abnormal floral development in Arabidopsis.Crossref | GoogleScholarGoogle Scholar |
Wang KS, Dong SS, Li FJ, Guo J, Tai SQ, Wang LB, Cheng DG, Mu P, Liu JJ, Li HS, Zhao ZD, Cao XY, Zhang YM (2020) QTL mapping and analysis of heading time and flowering time of wheat. Shandong Agriculture Science 52, 17–23.
Wen SY, Zhang Y, Deng Y, Chen GJ, Yu YX, Wei Q (2020) Genomic identification and expression analysis of the BBX transcription factor gene family in Petunia hybrida. Molecular Biology Reports 47, 6027–6041.
| Genomic identification and expression analysis of the BBX transcription factor gene family in Petunia hybrida.Crossref | GoogleScholarGoogle Scholar |
Wittkopp PJ, Kalay G (2012) Cis-regulatory elements: molecular mechanisms and evolutionary processes underlying divergence. Nature Reviews. Genetics 13, 59–69.
| Cis-regulatory elements: molecular mechanisms and evolutionary processes underlying divergence.Crossref | GoogleScholarGoogle Scholar |
Wu YF, Zhu ZG, Ma LG, Chen MS (2008) The preferential retention of starch synthesis genes reveals the impact of whole-genome duplication on grass evolution. Molecular Biology and Evolution 25, 1003–1006.
| The preferential retention of starch synthesis genes reveals the impact of whole-genome duplication on grass evolution.Crossref | GoogleScholarGoogle Scholar |
Xiong C, Luo D, Lin AH, Zhang CL, Shan LB, He P, Li B, Zhang QM, Hua B, Yuan ZL, Li HX, Zhang JH, Yang CX, Lu YG, Ye ZB, Wang TT (2019) A tomato B-box protein SlBBX20 modulates carotenoid biosynthesis by directly activating PHYTOENE SYNTHASE 1, and is targeted for 26S proteasome-mediated degradation. New Phytologist 221, 279–294.
| A tomato B-box protein SlBBX20 modulates carotenoid biosynthesis by directly activating PHYTOENE SYNTHASE 1, and is targeted for 26S proteasome-mediated degradation.Crossref | GoogleScholarGoogle Scholar |
Yan HL, Marquardt K, Indorf M, Jutt D, Kircher S, Neuhaus G, Rodriguezfranco M (2011) Nuclear localization and interaction with COP1 are required for STO/BBX24 function during photomorphogenesis. Plant Physiology 156, 1772–1782.
| Nuclear localization and interaction with COP1 are required for STO/BBX24 function during photomorphogenesis.Crossref | GoogleScholarGoogle Scholar |
Yang YJ, Ma C, Xu YJ, Wei Q, Imtiaz M, Lan H, Gao S, Cheng LN, Wang MY, Fei ZJ, Hong B, Gao J (2014) A zinc finger protein regulates flowering time and abiotic stress tolerance in Chrysanthemum by modulating gibberellin biosynthesis. The Plant Cell 26, 2038–2054.
| A zinc finger protein regulates flowering time and abiotic stress tolerance in Chrysanthemum by modulating gibberellin biosynthesis.Crossref | GoogleScholarGoogle Scholar |
Zhang Z, Li J, Zhao XQ, Wang J, Wong GK, Yu J (2006) KaKs_Calculator: calculating Ka and Ks through model selection and model averaging. Genomics, Proteomics & Bioinformatics 4, 259–263.
| KaKs_Calculator: calculating Ka and Ks through model selection and model averaging.Crossref | GoogleScholarGoogle Scholar |
Zhou XY, Zhu XG, Shao WS, Song JH, Jiang WQ, He YQ, Yin JL, Ma DF, Qiao Y (2020) Genome-wide mining of wheat DUF966 gene family provides new insights into salt stress responses. Frontiers in Plant Science 11, 569838
| Genome-wide mining of wheat DUF966 gene family provides new insights into salt stress responses.Crossref | GoogleScholarGoogle Scholar |
