Chin Bull Bot ›› 2017, Vol. 52 ›› Issue (6): 699-712.doi: 10.11983/CBB16244

• EXPERIMENTAL COMMUNICATIONS • Previous Articles     Next Articles

Genome-wide Survey and Phylogenetic Analysis of MADS-box Gene Family in Brassica napus

Gao Huhu, Zhang Yunxiao, Hu Shengwu, Guo Yuan*()   

  1. State Key Laboratory of Crop Stress Biology for Arid Areas, College of Agronomy, Northwest A&F University, Yangling 712100, China
  • Received:2016-12-12 Accepted:2017-05-22 Online:2017-11-22 Published:2017-11-01
  • Contact: Guo Yuan E-mail:guoyuan2109@163.com

Abstract:

The MADS-box gene family is involved in many processes during plant growth and development, such as flowering time, floral organ differentiation, root growth, meristem differentiation, ovary and gamete development, fruit enlargement and senescence. In this study, we used rape (Brassica napus) genome sequencing data with bioinformatics methods to identify and annotate the MADS-box genes. Rape contains 307 members of MADS-box gene family. According to the evolutionary relationships, these genes can be divided into two subfamilies: I-type, also known as M-type, containing three subclades, α, β, and γ; II type, also known as MIKC-type containing two subclades, MIKCC and MIKC*. MIKCC can be further divided into 13 groups. The number of MADS-box genes is greater in the A than C subgenome chromosome of B. napus. For the gene structure, the sequence is longer for MIKC-type than M-type genes and contains more exons. The number of motifs in M-type genes is about 2-5, and MIKC-type genes contain an average of 7 motifs. Synteny analysis revealed that whole-genome duplication played a major role in the expansion of the BnaMADS gene family, especially the MIKC-type subfamily. The selection pressure of the MIKC-type subfamily was about 2 times that for the M-type, which resulted in the selective preservation of MIKC-type subfamily genes during evolution.

Key words: Brassica napus, MADS-box, gene structure, evolution, synteny

Figure 1

Phylogenetic analysis of rapeseed, Arabidopsis and rice MADS-box genes(A) M-type; (B) MIKC-type"

Figure 2

Chromosomal location of MADS-box genes in Brassica napus"

Figure 3

Statistics of MADS-box genes in chromosome of Brassica napus"

Table 1

Distribution of MADS-box genes in subgenome of Brassica napus"

Subgenome M-type MIKC-type Total
A 55 85 140
C 52 77 129

Figure 4

Motif patterns of different MADS-box gene families in Brassica napus(A) MIKCC subfamily; (B) MIKC* subfamily; (C) M-type subfamily"

Figure 5

Distribution of MADS-box genes synteny with Arabidopsis thaliana in Brassica napus"

Figure 6

Syntenic relationship of MADS-box genes between Arabidopsis thaliana and Brassica napus"

Figure 7

Copy number of Arabidopsis thaliana MADS-box genes in Brassica napus"

Table 2

Select pressure of MADS-box gene subfamily in Brassica napus"

Subfamily Arabidopsis Brassica napus Average copy number Average Ka/Ks
thaliana
M-type 20 34 1.7 0.43
MIKC-type 29 95 3.27 0.22
[1] Airoldi CA, Davies B (2012). Gene duplication and the evolution of plant MADS-box transcription factors.J Genet Genomics 39, 157-165.
doi: 10.1016/j.jgg.2012.02.008 pmid: 22546537
[2] Alvarez-Buylla ER, Liljegren SJ, Pelaz S, Gold SE, Burgeff C, Ditta GS, Vergara-Silva F, Yanofsky MF (2000a). MADS-box gene evolution beyond flowers: expres- sion in pollen, endosperm, guard cells, roots and trichom- es.Plant J 24, 457-466.
doi: 10.1046/j.1365-313x.2000.00891.x
[3] Alvarez-Buylla ER, Pelaz S, Liljegren SJ, Gold SE, Bur- geff C, Ditta GS, de Pouplana LR, Martínez-Castilla L, Yanofsky MF (2000b). An ancestral MADS-box gene duplication occurred before the divergence of plants and animals.Proc Natl Acad Sci USA 97, 5328-5333.
doi: 10.1073/pnas.97.10.5328
[4] Arora R, Agarwal P, Ray S, Singh AK, Singh VP, Tyagi AK, Kapoor S (2007). MADS-box gene family in rice: genome-wide identification, organization and expression profiling during reproductive development and stress.BMC Genomics 8, 242.
doi: 10.1186/1471-2164-8-242 pmid: 17640358
[5] Bowers JE, Chapman BA, Rong JK, Paterson AH (2003). Unravelling angiosperm genome evolution by phylogene- tic analysis of chromosomal duplication events.Nature 422, 433-438.
doi: 10.1038/nature01521
[6] Chalhoub B, Denoeud F, Liu SY, Parkin IAP, Tang HB, Wang XY, Chiquet J, Belcram H, Tong C, Samans B, Corréa M, Da Silva C, Just J, Falentin C, Koh CS, Le Clainche I, Bernard M, Bento P, Noel B, Labadie K, Alberti A, Charles M, Arnaud D, Guo H, Daviaud C, Alamery S, Jabbari K, Zhao MX, Edger PP, Chelaifa H, Tack D, Lassalle G, Mestiri I, Schnel N, Le Paslier MC, Fan GY, Renault V, Bayer PE, Golicz AA, Manoli S, Lee TH, Thi VHD, Chalabi S, Hu Q, Fan CC, Tollenaere R, Lu YH, Battail C, Shen JX, Sidebottom CHD, Wang XF, Canaguier A, Chauveau A, Bérard A, Deniot G, Guan M, Liu ZS, Sun FM, Lim YP, Lyons E, Town CD, Bancroft I, Wang XW, Meng JL, Ma JX, Pires JC, King GJ, Brunel D, Delourme R, Renard M, Aury JM, Adams KL, Batley J, Snowdon RJ, Tost J, Edwards D, Zhou YM, Hua W, Sharpe AG, Paterson AH, Guan CY, Wincker P (2014). Early allopolyploid evolution in the post- Neolithic Brassica napus oilseed genome. Science 345, 950-953.
[7] Chang YY, Chiu YF, Wu JW, Yang CH (2009). Four orchid (Oncidium Gower Ramsey) AP1/AGL9-like MADS box genes show novel expression patterns and cause different effects on floral transition and formation in Arabidopsis thaliana. Plant Cell Physiol 50, 1425-1438.
[8] Cheng F, Liu SY, Wu J, Fang L, Sun SL, Liu B, Li PX, Hua W, Wang XW (2011). BRAD, the genetics and genomics database for Brassica plants. BMC Plant Biol 11, 136.
doi: 10.1186/1471-2229-11-136 pmid: 21995777
[9] Day RC, Herridge RP, Ambrose BA, Macknight RC (2008). Transcriptome analysis of proliferating Arabidopsis endos- perm reveals biological implications for the control of syn- cytial division, cytokinin signaling, and gene expression regulation.Plant Physiol 148, 1964-1984.
doi: 10.4161/psb.4.9.9461 pmid: 18923020
[10] De Bodt S, Raes J, Van de Peer Y, Thei?en G (2003). And then there were many: MADS goes genomic.Trends Plant Sci 8, 475-483.
doi: 10.1016/j.tplants.2003.09.006 pmid: 14557044
[11] Díaz-Riquelme J, Lijavetzky D, Martínez-Zapater JM, Carmona MJ (2009). Genome-wide analysis of MIKCC- type MADS box genes in grapevine.Plant Physiol 149, 354-369.
doi: 10.1104/pp.108.131052
[12] Doebley J, Lukens L (1998). Transcriptional regulators and the evolution of plant form.Plant Cell 10, 1075-1082.
doi: 10.2307/3870712 pmid: 9668128
[13] Duan WK, Song XM, Liu TK, Huang ZN, Ren J, Hou XL, Li Y (2015). Genome-wide analysis of the MADS-box gene family in Brassica rapa (Chinese cabbage). Mol Genet Genomics 290, 239-255.
doi: 10.1007/s00438-014-0912-7 pmid: 25216934
[14] Edger PP, Pires JC (2009). Gene and genome duplications: the impact of dosage-sensitivity on the fate of nuclear genes.Chromosome Res 17, 699-717.
doi: 10.1007/s10577-009-9055-9
[15] Fan CM, Wang X, Wang YW, Hu RB, Zhang XM, Chen JX, Fu YF (2013). Genome-wide expression analysis of soy- bean MADS genes showing potential function in the seed development.PLoS One 8, e62288.
doi: 10.1371/journal.pone.0062288 pmid: 23638026
[16] Fang SC, Fernandez DE (2002). Effect of regulated over- expression of the MADS domain factor AGL15 on flower senescence and fruit maturation.Plant Physiol 130, 78-89.
doi: 10.1104/pp.004721 pmid: 12226488
[17] Finn RD, Bateman A, Clements J, Coggill P, Eberhardt RY, Eddy SR, Heger A, Hetherington K, Holm L, Mistry J, Sonnhammer ELL, Tate J, Punta M (2014). Pfam: the protein families database.Nucleic Acids Res 42, D222-D230.
doi: 10.1093/nar/gkt1223 pmid: 3965110
[18] Gan YB, Filleur S, Rahman A, Gotensparre S, Forde BG (2005). Nutritional regulation of ANR1 and other root- expressed MADS-box genes in Arabidopsis thaliana. Planta 222, 730-742.
[19] Gramzow L, Ritz MS, Thei?en G (2010). On the origin of MADS-domain transcription factors.Trends Genet 26, 149-153.
doi: 10.1016/j.tig.2010.01.004 pmid: 20219261
[20] Greenup A, Peacock WJ, Dennis ES, Trevaskis B (2009). The molecular biology of seasonal flowering-responses in Arabidopsis and the cereals.Ann Bot 103, 1165-1172.
doi: 10.1093/aob/mcp063 pmid: 2685306
[21] Grimplet J, Martínez-Zapater JM, Carmona MJ (2016). Structural and functional annotation of the MADS-box transcription factor family ingrapevine.BMC Genomics 17, 80.
doi: 10.1186/s12864-016-2398-7 pmid: 4729134
[22] Hemming MN, Trevaskis B (2011). Make hay when the sun shines: the role of MADS-box genes intemperature- dependant seasonal flowering responses.Plant Sci 180, 447-453.
doi: 10.1016/j.plantsci.2010.12.001 pmid: 21421391
[23] Immink RGH, Kaufmann K, Angenent GC (2010). The ‘ABC’ of MADS domain protein behaviour and interactions.Semin Cell Dev Biol 21, 87-93.
doi: 10.1016/j.semcdb.2009.10.004 pmid: 19883778
[24] Jin JP, Zhang H, Kong L, Gao G, Luo JC (2014). Plant TFDB 3.0: a portal for the functional and evolutionary study of plant transcription factors.Nucleic Acids Res 42, D1182-D1187.
doi: 10.1093/nar/gkt1016 pmid: 24174544
[25] Kawahara Y, de la Bastide M, Hamilton JP, Kanamori H, McCombie WR, Ouyang S, Schwartz DC, Tanaka T, Wu JZ, Zhou SG, Childs KL, Davidson RM, Lin HN, Quesada-Ocampo L, Vaillancourt B, Sakai H, Lee SS, Kim J, Numa H, Itoh T, Buell CR, Matsumoto T (2013). Improvement of the Oryza sativa Nipponbare reference genome using next generation sequence and optical map data. Rice 6, 4.
doi: 10.1186/1939-8433-6-4 pmid: 24280374
[26] Kofuji R, Sumikawa N, Yamasaki M, Kondo K, Ueda K, Ito M, Hasebe M (2003). Evolution and divergence of the MADS-box gene family based on genome-wide expression analyses.Mol Biol Evol 20, 1963-1977.
doi: 10.1093/molbev/msg216 pmid: 12949148
[27] Krzywinski M, Schein J, Birol I, Connors J, Gascoyne R, Horsman D, Jones SJ, Marra MA (2009). Circos: an information aesthetic for comparative genomics.Genome Res 19, 1639-1645.
doi: 10.1101/gr.092759.109
[28] Letunic I, Doerks T, Bork P (2015). SMART: recent upda- tes, new developments and status in 2015.Nucleic Acids Res 43, D257-D260.
doi: 10.1093/nar/gku949 pmid: 25300481
[29] Liu SY, Liu YM, Yang XH, Tong CB, Edwards D, Parkin IAP, Zhao MX, Ma JX, Yu JY, Huang SM, Wang XY, Wang JY, Lu K, Fang ZY, Bancroft I, Yang TJ, Hu Q, Wang XF, Yue Z, Li HJ, Yang LF, Wu J, Zhou Q, Wang WX, King GJ, Pires JC, Lu CX, Wu ZY, Sampath P, Wang Z, Guo H, Pan SK, Yang LM, Min JM, Zhang D, Jin DC, Li WS, Belcram H, Tu JX, Guan M, Qi CK, Du DZ, Li JN, Jiang LC, Batley J, Sharpe AG, Park BS, Ruperao P, Cheng F, Waminal NE, Huang Y, Dong CH, Wang L, Li JP, Hu ZY, Zhuang M, Huang Y, Huang JY, Shi JQ, Mei DS, Liu J, Lee TH, Wang JP, Jin HZ, Li ZY, Li X, Zhang JF, Xiao L, Zhou YM, Liu ZS, Liu XQ, Qin R, Tang X, Liu WB, Wang YP, Zhang YY, Lee J, Kim HH, Denoeud F, Xu X, Liang XM, Hua W, Wang XW, Wang J, Chalhoub B, Paterson AH (2014). The Brassica oleracea genome reveals the asymmetrical evolution of polyploid genomes. Nat Commun 5, 3930.
[30] Liu Y, Cui SJ, Wu F, Yan S, Lin XL, Du XQ, Chong K, Schilling S, Thei?en G, Meng Z (2013). Functional con- servation of MIKC*-type MADS box genes in Arabidopsis and rice pollen maturation.Plant Cell 25, 1288-1303.
doi: 10.1105/tpc.113.110049
[31] Maere S, De Bodt S, Raes J, Casneuf T, Van Montagu M, Kuiper M, Van de Peer Y (2005). Modeling gene and genome duplications in eukaryotes.Proc Natl Acad Sci USA 102, 5454-5459.
doi: 10.1073/pnas.0501102102
[32] Masiero S, Colombo L, Grini PE, Schnittger A, Kater MM (2011). The emerging importance of type I MADS box transcription factors for plant reproduction.Plant Cell 23, 865-872.
doi: 10.1105/tpc.110.081737 pmid: 21378131
[33] Mitchell A, Chang HY, Daugherty L, Fraser M, Hunter S, Lopez R, McAnulla C, McMenamin C, Nuka G, Pesseat S, Sangrador-Vegas A, Scheremetjew M, Rato C, Yong SY, Bateman A, Punta M, Attwood TK, Sigrist CJA, Redaschi N, Rivoire C, Xenarios I, Kahn D, Guyot D, Bork P, Letunic I, Gough J, Oates M, Haft D, Huang HZ, Natale DA, Wu CH, Orengo C, Sillitoe I, Mi HY, Thomas PD, Finn RD (2015). The InterPro protein families data- base: the classification resource after 15 years.Nucleic Acids Res 43, D213-D221.
doi: 10.1093/nar/gku1243 pmid: 4383996
[34] Nagaharu U (1935). Genome analysis in Brassica with spe- cial reference to the experimental formation of B. napus and peculiar mode of fertilization. Jpn J Bot 7, 389-452.
[35] Nakano T, Suzuki K, Fujimura T, Shinshi H (2006). Genome- wide analysis of the ERF gene family in Arabidopsis and rice.Plant Physiol 140, 411-432.
doi: 10.1104/pp.105.073783
[36] Nam J, dePamphilis CW, Ma H, Nei M (2003). Antiquity and evolution of the MADS-box gene family controlling flower development in plants.Mol Biol Evol 20, 1435-1447.
doi: 10.1093/molbev/msg152 pmid: 12777513
[37] Parenicová L, de Folter S, Kieffer M, Horner DS, Favalli C, Busscher J, Cook HE, Ingram RM, Kater MM, Davies B, Angenent GC, Colombo L (2003). Molecular and phylo- genetic analyses of the complete MADS-box transcription factor family in Arabidopsis: new openings to the MADS world.Plant Cell 15, 1538-1551.
doi: 10.1105/tpc.011544
[38] Purugganan MD, Rounsley SD, Schmidt RJ, Yanofsky MF (1995). Molecular evolution of flower development: diver- sification of the plant MADS-box regulatory gene family.Genetics 140, 345-356.
[39] Saha G, Park JI, Jung HJ, Ahmed NU, Kayum MA, Chung MY, Hur Y, Cho YG, Watanabe M, Nou IS (2015). Genome-wide identification and characterization of MADS- box family genes related to organ development and stress resistance in Brassica rapa. BMC Genomics 16, 178.
doi: 10.1186/s12864-015-1349-z pmid: 4422603
[40] Shao SQ, Li BY, Zhang ZT, Zhou Y, Jiang J, Li XB (2010). Expression of a cotton MADS-box gene is regulated in anther development and in response to phytohormone sig- naling.J Genet Genomics 37, 805-816.
doi: 10.1016/S1673-8527(09)60098-9 pmid: 21193159
[41] Shore P, Sharrocks AD (1995). The MADS-box family of transcription factors.Eur J Biochem 229, 1-13.
doi: 10.1111/j.1432-1033.1995.0001l.x pmid: 7744019
[42] Shu YJ, Yu DS, Wang D, Guo DL, Guo CH (2013). Genome- wide survey and expression analysis of the MADS-box gene family in soybean.Mol Biol Rep 40, 3901-3911.
doi: 10.1007/s11033-012-2438-6 pmid: 23559340
[43] Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013). MEGA6: molecular evolutionary genetics analysis version 6.0.Mol Biol Evol 30, 2725-2729.
doi: 10.1093/molbev/mst197
[44] Tang HB, Bowers JE, Wang XY, Ming R, Alam M, Pater- son AH (2008). Synteny and collinearity in plant genomes.Science 320, 486-488.
doi: 10.1126/science.1153917 pmid: 18436778
[45] Tapia-López R, García-Ponce B, Dubrovsky JG, Garay- Arroyo A, Pérez-Ruíz RV, Kim SH, Acevedo F, Pelaz S, Alvarez-Buylla ER (2008). An AGAMOUS-related MADS- box gene, XAL1 (AGL12), regulates root meristem cell proliferation and flowering transition in Arabidopsis. Plant Physiol 146, 1182-1192.
[46] The Brassica rapa Genome Sequencing Project Con- sortium, Wang XW, Wang HZ, Wang J, Sun RF, Wu J, Liu SY, Bai YQ, Mun JH, Bancroft I, Cheng F, Huang SW, Li XX, Hua W, Wang JY, Wang XY, Freeling M, Pires JC, Paterson AH, Chalhoub B, Wang B, Hayward A, Sharpe AG, Park BS, Weisshaar B, Liu BH, Li B, Liu B, Tong CB, Song C, Duran C, Peng CF, Geng CY, Koh C, Lin CY, Edwards D, Mu DS, Shen D, Soumpourou E, Li F, Fraser F, Conant G, Lassalle G, King GJ, Bonn- ema G, Tang HB, Wang HP, Belcram H, Zhou HL, Hirakawa H, Abe H, Guo H, Wang H, Jin HZ, Parkin IAP, Batley J, Kim JS, Just J, Li JW, Xu JH, Deng J, Kim JA, Li JP, Yu JY, Meng JL, Wang JP, Min JM, Poulain J, Wang J, Hatakeyama K, Wu K, Wang L, Fang L, Trick M, Links MG, Zhao MX, Jin MN, Ramchiary N, Drou N, Berkman PJ, Cai QL, Huang QF, Li RQ, Tabata S, Cheng SF, Zhang S, Zhang SJ, Huang SM, Sato SS, Sun SL, Kwon SJ, Choi SR, Lee TH, Fan W, Zhao X, Tan X, Xu X, Wang Y, Qiu Y, Yin Y, Li YR, Du YC, Liao YC, Lim Y, Narusaka Y, Wang YP, Wang ZY, Li ZY, Wang ZW, Xiong ZY, Zhang ZH (2011). The genome of the mesopolyploid crop species Brassica rapa. Nat Genet 43, 1035-1039.
[47] Theissen G, Becker A, Di Rosa A, Kanno A, Kim JT, Münster T, Winter KU, Saedler H (2000). A short history of MADS-box genes in plants.Plant Mol Biol 42, 115-149.
doi: 10.1023/A:1006332105728 pmid: 10688133
[48] Tiwari S, Spielman M, Schulz R, Oakey RJ, Kelsey G, Salazar A, Zhang K, Pennell R, Scott RJ (2010). Trans- criptional profiles underlying parent-of-origin effects in seeds of Arabidopsis thaliana. BMC Plant Biol 10, 72.
[49] Wei B, Zhang RZ, Guo JJ, Liu DM, Li AL, Fan RC, Mao L, Zhang XQ (2014). Genome-wide analysis of the MADS- box gene family in Brachypodium distachyon. PLoS One 9, e84781.
[50] Wei X, Wang LH, Yu JY, Zhang YX, Li DH, Zhang XR (2015). Genome-wide identification and analysis of the MADS-box gene family insesame.Gene 569, 66-76.
doi: 10.1016/j.gene.2015.05.018 pmid: 25967387
[51] Woodhouse MR, Cheng F, Pires JC, Lisch D, Freeling M, Wang XW (2014). Origin, inheritance, and gene regulatory consequences of genome dominance in polyploids.Proc Natl Acad Sci USA 111, 5283-5288.
doi: 10.1073/pnas.1402475111 pmid: 24706847
[52] Wuest SE, Vijverberg K, Schmidt A, Weiss M, Gheyse- linck J, Lohr M, Wellmer F, Rahnenführer J, von Mering C, Grossniklaus U (2010). Arabidopsis female gametophyte gene expression map reveals similarities bet- ween plant and animal gametes.Curr Biol 20, 506-512.
doi: 10.1016/j.cub.2010.01.051 pmid: 20226671
[53] Xu ZD, Zhang QX, Sun LD, Du DL, Cheng TR, Pan HT, Yang WR, Wang J (2014). Genome-wide identification, characterisation and expression analysis of the MADS-box gene family in Prunus mume. Mol Genet Genomics 289, 903-920.
doi: 10.1007/s00438-014-0863-z pmid: 24859011
[54] Yang JH, Liu DY, Wang XW, Ji CM, Cheng F, Liu BN, Hu ZY, Chen S, Pental D, Ju YH, Yao P, Li XM, Xie K, Zhang JH, Wang JL, Liu F, Ma WW, Shopan J, Zheng HK, Mackenzie SA, Zhang MF (2016). The genome se- quence of allopolyploid Brassica juncea and analysis of differential homoeolog gene expression influencing selec- tion. Nat Genet 48, 1225-1232.
[55] Yanofsky MF, Ma H, Bowman JL, Drews GN, Feldmann KA, Meyerowitz EM (1990). The protein encoded by the Arabidopsis homeotic gene AGAMOUS resembles trans- cription factors. Nature 346, 35-39.
[56] Yao QY, Xia EH, Liu FH, Gao LZ (2015). Genome-wide identification and comparative expression analysis reveal a rapid expansion and functional divergence of duplicated genes in the WRKY gene family of cabbage, Brassica oleracea var. capitata. Gene 557, 35-42.
doi: 10.1016/j.gene.2014.12.005 pmid: 25481634
[57] Yu LH, Miao ZQ, Qi GF, Wu J, Cai XT, Mao JL, Xiang CB (2014). MADS-box transcription factor AGL21 regulates lateral root development and responds to multiple external and physiological signals.Mol Plant 7, 1653-1669.
doi: 10.1093/mp/ssu088 pmid: 4228986
[58] Zhang Z, Li J, Zhao XQ, Wang J, Wong GKS, Yu J (2006). KaKs_calculator: calculating Ka and Ks through model selection and model averaging.Genomics Proteomics Bioinformatics 4, 259-263.
doi: 10.1016/S1672-0229(07)60007-2 pmid: 5054075
[1] Zuo zeyuan. Gene evolution and functional analysis of cluster characteristics in anther development of Arabidopsis thaliana [J]. Chin Bull Bot, 2020, 55(2): 0-0.
[2] Lu Ningna, Liu Zhenheng, Ma Yan, Lu Guangmei, Meng Xiuxiang. Phenotypic selection analysis of flower traits in Delphinium kamaonense var. glabrescens (Ranunculaceae) [J]. Biodiv Sci, 2019, 27(7): 772-777.
[3] Song Min,Zhang Yao,Wang Liying,Peng Xiangyong. Genome-wide Identification and Phylogenetic Analysis of Zinc Finger Homeodomain Family Genes in Brassica napus [J]. Chin Bull Bot, 2019, 54(6): 699-710.
[4] Tu Weifeng,Zhang Yang,Tang Jie,Tu Yuqin,Xin Jiajia,Ji Hongli,Zhang Nanfeng,Zhang Tao. Comparison of taxonomic morphological characteristics between Rorippa indica and R. dubia [J]. Biodiv Sci, 2019, 27(2): 168-176.
[5] Hao Wang, Rui Zhang, Jiao Zhang, Hui Shen, Xiling Dai, Yuehong Yan. De novo transcriptome assembly reveals the whole genome duplication events of Didymochlaena trancatula [J]. Biodiv Sci, 2019, 27(11): 1221-1227.
[6] Guohua Zhao, Ying Wang, Hui Shang, Xile Zhou, Aihua Wang, Yufeng Li, Hui Wang, Baodong Liu, Yuehong Yan. Ancestral state reconstruction reveals the diversity and evolution of spore ornamentation in Adiantum (Pteridaceae) [J]. Biodiv Sci, 2019, 27(11): 1228-1235.
[7] Jinxiu Ke,Duo Chen,Yanping Guo. Designing leaf marginal shapes: Regulatory mechanisms of leaf serration or dissection [J]. Biodiv Sci, 2018, 26(9): 988-997.
[8] TAN Ke, DONG Shu-Peng, LU Tao, ZHANG Ya-Jing, XU Shi-Tao, REN Ming-Xun. Diversity and evolution of samara in angiosperm [J]. Chin J Plan Ecolo, 2018, 42(8): 806-817.
[9] Shaoshuai Yu, Caili Lin, Shengjie Wang, Wenxin Zhang, Guozhong Tian. Structures of the tuf gene and its upstream part genes and characteristic analysis of conserved regions and activity from related gene promoters of a phytoplasma [J]. Biodiv Sci, 2018, 26(7): 738-748.
[10] Hou Qinxi, Ci Xiuqin, Liu Zhifang, Xu Wumei, Li Jie. Assessment of the evolutionary history of Lauraceae in Xishuangbanna National Nature Reserve using DNA barcoding [J]. Biodiv Sci, 2018, 26(3): 217-228.
[11] Zhigang Jiang,Lili Li,Yiming Hu,Huijian Hu,Chunwang Li,Xiaoge Ping,Zhenhua Luo. Diversity and endemism of ungulates on the Qinghai-Tibetan Plateau: Evolution and conservation [J]. Biodiv Sci, 2018, 26(2): 158-170.
[12] ZHAOLe-Wen, CHEN Zi-Yi, ZOU Ying, FU Zi-Zhao, WU Gui-Lin, LIU Xiao-Rong, LUO Qi, LIN Yi-Xue, LI Xiong-Ju, LIU Zhi-Tong, LIU Hui. Changes in hydraulic traits of nine vascular plants from different evolutionary lineages [J]. Chin J Plan Ecolo, 2018, 42(2): 220-228.
[13] Jibao Jiang, Jiangping Qiu. Origin and evolution of earthworms belonging to the family Megascolecidae in China [J]. Biodiv Sci, 2018, 26(10): 1074-1082.
[14] Jun-Wei YE, Yang ZHANG, Xiao-Juan WANG. Phylogeographic breaks and the mechanisms of their formation in the Sino-Japanese floristic region [J]. Chin J Plan Ecolo, 2017, 41(9): 1003-1019.
[15] Liu Kaige, Qi Shuanghui, Duan Shaowei, Li Dong, Jin Changyu, Gao Chenhao, Liu Mingxun Chen Xuanxia. Functional Analysis of Brassica napus BnTTG1-1 Gene [J]. Chin Bull Bot, 2017, 52(6): 713-722.
Viewed
Full text


Abstract

Cited

  Shared   
  Discussed   
[1] . [J]. Chin Bull Bot, 1994, 11(专辑): 19 .
[2] Xiao Xiao and Cheng Zhen-qi. Chloroplast 4.5 S ribosomol DNA. II Gene and Origin[J]. Chin Bull Bot, 1985, 3(06): 7 -9 .
[3] CAO Cui-LingLI Sheng-Xiu. Effect of Nitrogen Level on the Photosynthetic Rate, NR Activity and the Contents of Nucleic Acid of Wheat Leaf in the Stage of Reproduction[J]. Chin Bull Bot, 2003, 20(03): 319 -324 .
[4] SONG Li-Ying TAN Zheng GAO Feng DENG Shu-Yan. Advances in in vitro Culture of Cucurbitaceae in China[J]. Chin Bull Bot, 2004, 21(03): 360 -366 .
[5] Shi Jian ming;Gui Yao-lin and Zhu Zhi-qing. Observation on Amitosis of Sugarbeet (Beta vulgaris) Petiole during Dedifferentiation in Vitro[J]. Chin Bull Bot, 1989, 6(03): 155 .
[6] LI Jun-De YANG Jian WANG Yu-Fei. Aquatic Plants in the Miocene Shanwang Flora[J]. Chin Bull Bot, 2000, 17(专辑): 261 .
[7] XU Jing-Xian WANG Yu-Fei YANG Jian PU Guang-Rong ZHANG Cui-Fen. Advances in the Research of Tertiary Flora and Climate in Yunnan[J]. Chin Bull Bot, 2000, 17(专辑): 84 -94 .
[8] Sun Zhen-xiao Xia Guang-min Chen Hui-min. Karyotype Analysis of Psathyrostachys juncea[J]. Chin Bull Bot, 1995, 12(01): 56 .
[9] . [J]. Chin Bull Bot, 1994, 11(专辑): 8 -9 .
[10] Yunpu Zheng;Jiancheng Zhao * ;Bingchang Zhang;Lin Li;Yuanming Zhang . Advances on Ecological Studies of Algae and Mosses in Biological Soil Crust[J]. Chin Bull Bot, 2009, 44(03): 371 -378 .