高级检索

Sciences in Cold and Arid Regions ›› 2018, Vol. 10 ›› Issue (5): 428–435.doi: 10.3724/SP.J.1226.2018.00428

• • 上一篇    下一篇

  

  • 收稿日期:2018-04-16 接受日期:2018-08-15 出版日期:2018-11-19 发布日期:2018-11-21
  • 基金资助:
    This work was supported by National Natural Science Foundation of China (No. 41201048) and by the Youth Innovation Promotion Association of Chinese Academy of Sciences (2018463).

Transcriptomic comparison to identify rapidly evolving genes in Braya humilis

YuMing Wei1,XiaoFei Ma2,PengShan Zhao2,*()   

  1. 1 Animal Husbandry Pasture and Green Agriculture Institute of Gansu Academy of Agricultural Sciences, Lanzhou, Gansu 730070, China
    2 Key Laboratory of Stress Physiology and Ecology in Cold and Arid Regions, Northwest Institute of Eco-Environment and Resources, Chinese Academy of Sciences, Lanzhou, Gansu 730000, China
  • Received:2018-04-16 Accepted:2018-08-15 Online:2018-11-19 Published:2018-11-21
  • Contact: PengShan Zhao E-mail:zhaopengshan@lzb.ac.cn
  • Supported by:
    This work was supported by National Natural Science Foundation of China (No. 41201048) and by the Youth Innovation Promotion Association of Chinese Academy of Sciences (2018463).

RichHTML

18

PDF (PC)

307

Abstract:

The Brassicaceae species Braya humilis shows broad adaptation to different climatic zones and latitudes. However, the molecular adaptation mechanism of B. humilis is poorly understood. In China, B. humilis is mainly distributed on the Qinghai-Tibetan Plateau (QTP) and in the adjacent arid region. Previous transcriptome analysis of B. humilis has revealed that 39 salt and osmotic stress response genes are subjected to purifying selection during its speciation. To further explore the adaptation mechanism of B. humilis to an arid environment, OrthoMCL program was employed in this study and 6,268 pairs of orthologous gene pairs with high confidence were obtained betweenB. humilis and Arabidopsis thaliana. A comparative evolutionary analysis based on nonsynonymous to synonymous substitution ratio (Ka/Ks) was then conducted. There were 64 pairs exhibiting a Ka/Ks ratio more than 0.5 and among which, three instrumental candidate genes, T2_20487, T2_22576, and T2_13757, were identified with strong selection signatures (Ka/Ks >1). The corresponding A. thaliana orthologs are double-stranded RNA-binding domain protein, MADS-box family protein, and NADH-dehydrogenase subunit 6, which is encoded by mitochondria genome. This report not only demonstrates the adaptation contribution of fast evolving nuclear genes, but also highlights the potential adaptive value of mitochondria gene to the speciation and adaptation of B. humilis toward the extreme environment in an arid region.

Key words: Braya humilis, positive selection, Ka/Ks, mitochondria gene variation, NADH-dehydrogenase subunit 6

"

"

"

Ortholog ID Arabidopsis gene B. humilis gene Ka Ks Ka/Ks Annotation
OG10864 At|ATMG00270.1 Bh|T2_13757 0.021 0.017 1.216 NADH dehydrogenase subunit 6 (NAD6)
OG08423 At|AT4G00420.2 Bh|T2_20487 0.125 0.118 1.063 Double-stranded RNA-binding domain (DsRBD)-containing protein
OG07470 At|AT3G12510.1 Bh|T2_22576 0.157 0.153 1.023 MADS-box family protein
OG08984 At|AT4G28160.1 Bh|T2_14710 0.186 0.210 0.885 Hydroxyproline-rich glycoprotein family protein
OG10866 At|ATMG00830.1 Bh|T2_8533 0.024 0.028 0.867 Cytochrome c biogenesis biogenesis 382 (CCB382)
OG07331 At|AT3G07525.2 Bh|T2_11702 0.061 0.073 0.838 AUTOPHAGY 10 (ATG10)
OG07729 At|AT3G21000.1 Bh|T2_30213 0.142 0.185 0.769 Gag-Pol-related retrotransposon family protein
OG06437 At|AT2G20620.1 Bh|T2_29281 0.181 0.236 0.768 Hypothetical protein
OG05855 At|AT1G69588.1 Bh|T2_23885 0.096 0.131 0.737 CLAVATA3/ESR-Related 45 (CLE45)
OG10748 At|AT5G64680.3 Bh|T2_26444 0.222 0.304 0.730 Mediator-associated protein
OG05953 At|AT1G73490.2 Bh|T2_4714 0.248 0.342 0.726 RNA-binding (RRM/RBD/RNP motifs) family protein
OG10862 At|ATMG00070.1 Bh|T2_18626 0.010 0.014 0.704 NADH dehydrogenase subunit 9 (NAD9)
OG07972 At|AT3G46910.1 Bh|T2_11373 0.135 0.194 0.698 Cullin family protein
OG08608 At|AT4G12100.1 Bh|T2_25782 0.158 0.233 0.679 Cullin family protein
OG08323 At|AT3G59550.1 Bh|T2_1079 0.099 0.145 0.678 Sister Chromatid Cohesion1 1
OG05765 At|AT1G67025.1 Bh|T2_40572 0.258 0.382 0.674 Wall-associated receptor kinase carboxy-terminal protein
OG05646 At|AT1G60700.1 Bh|T2_10793 0.074 0.110 0.674 SMAD/FHA domain-containing protein
OG07674 At|AT3G19150.1 Bh|T2_37031 0.093 0.140 0.666 Kip-related protein 6 (KRP6)
OG07898 At|AT3G28230.2 Bh|T2_19666 0.113 0.174 0.649 Something about silencing protein
OG09161 At|AT4G34530.1 Bh|T2_30131 0.064 0.099 0.644 Cryptochrome-interacting basic-helix-loop-helix 1 (CIB1)
OG05689 At|AT1G63245.1 Bh|T2_15034 0.192 0.303 0.635 CLAVATA3/ESR-Related 14 (CLE14)
OG06478 At|AT2G22000.1 Bh|T2_17745 0.079 0.126 0.632 Elicitor peptide 6 precursor
OG09339 At|AT5G01940.1 Bh|T2_26401 0.067 0.106 0.628 EIF-2B family protein
OG08306 At|AT3G58850.1 Bh|T2_18718 0.048 0.077 0.618 Phytochrome Rapidly Regulated2 (PAR2)
OG06953 At|AT2G41360.1 Bh|T2_18958 0.114 0.187 0.611 Galactose oxidase/kelch repeat protein
OG07249 At|AT3G04800.1 Bh|T2_36362 0.089 0.145 0.609 Translocase inner membrane subunit 23-3 (TIM23-3)
OG06515 At|AT2G24350.1 Bh|T2_2266 0.079 0.131 0.604 RNA binding (RRM/RBD/RNP motifs) family protein
OG10863 At|ATMG00180.1 Bh|T2_15220 0.033 0.056 0.596 Cytochrome c biogenesis 452 (CCB452)
OG08477 At|AT4G02310.1 Bh|T2_23130 0.143 0.241 0.592 Galactose oxidase/kelch repeat superfamily protein
OG05580 At|AT1G55260.1 Bh|T2_24979 0.078 0.133 0.583 Lipid-transfer protein 6 (LTPG6)
OG06781 At|AT2G35140.1 Bh|T2_36395 0.112 0.193 0.581 Development and Cell Death protein (DCD)
OG07825 At|AT3G25080.1 Bh|T2_11865 0.102 0.176 0.580 Hypothetical protein
OG08827 At|AT4G21550.1 Bh|T2_27886 0.066 0.117 0.564 VP1/ABI3-like 3 (VAL3)
OG04784 At|AT1G08060.1 Bh|T2_38418 0.088 0.157 0.560 MORPHEUS MOLECULE 1 (MOM1)

"

1 Al-Shehbaz IA, O'Kane Jr SL Arabidopsis gamosepala and A. tuemurnica belong to Neotorularia (Brassicaceae). Novon 1997; 7: 2 93- 94.
doi: 10.2307/3392176
2 Atkin OK, Macherel D The crucial role of plant mitochondria in orchestrating drought tolerance. Annals of Botany 2009; 103: 4 581- 597.
doi: 10.1093/aob/mcn094
3 Bock DG, Andrew RL, Rieseberg LH On the adaptive value of cytoplasmic genomes in plants. Molecular Ecology 2014; 23: 20 4899- 4911.
doi: 10.1111/mec.12920
4 Castresana J Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Molecular Biology and Evolution 2000; 17: 4 540- 552.
doi: 10.1093/oxfordjournals.molbev.a026334
5 Chatr-Aryamontri A, Breitkreutz BJ, Oughtred R, et al. The BioGRID interaction database: 2015 update. Nucleic Acids Research 2015; 43: Database issue D470- D478.
doi: 10.1093/nar/gku1204
6 Chaves MM, Flexas J, Pinheiro C Photosynthesis under drought and salt stress: regulation mechanisms from whole plant to cell. Annals of Botany 2009; 103: 4 551- 560.
doi: 10.1093/aob/mcn125
7 Chen LY, Zhao SY, Wang QF, et al. Transcriptome sequencing of three Ranunculus species (Ranunculaceae) reveals candidate genes in adaptation from terrestrial to aquatic habitats . Scientific Reports 2015; 5: 10098.
doi: 10.1038/srep10098
8 Comella P, Pontvianne F, Lahmy S, et al. Characterization of a ribonuclease III-like protein required for cleavage of the pre-rRNA in the 3'ETS in Arabidopsis . Nucleic Acids Research 2008; 36: 4 1163- 1175.
doi: 10.1093/nar/gkm1130
9 Couvreur TLP, Franzke A, Al-Shehbaz IA, et al. Molecular phylogenetics, temporal diversification, and principles of evolution in the mustard family (Brassicaceae). Molecular Biology and Evolution 2010; 27: 1 55- 71.
doi: 10.1093/molbev/msp202
10 Culligan KM, Robertson CE, Foreman J, et al. ATR and ATM play both distinct and additive roles in response to ionizing radiation. The Plant Journal 2006; 48: 6 947- 961.
doi: 10.1111/j.1365-313X.2006.02931.x
11 Edgar RC MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Research 2004; 32: 5 1792- 1797.
doi: 10.1093/nar/gkh340
12 Franzke A, Lysak MA, Al-Shehbaz IA, et al. Cabbage family affairs: the evolutionary history of Brassicaceae. Trends in Plant Science 2011; 16: 2 108- 116.
doi: 10.1016/j.tplants.2010.11.005
13 Greiner S, Bock R Tuning a menage a trois: co-evolution and co-adaptation of nuclear and organellar genomes in plants. BioEssays 2013; 35: 4 354- 365.
doi: 10.1002/bies.201200137
14 Hiraguri A, Itoh R, Kondo N, et al. Specific interactions between Dicer-like proteins and HYL1/DRB-family dsRNA-binding proteins in Arabidopsis thaliana . Plant Molecular Biology 2005; 57: 2 173- 188.
doi: 10.1007/s11103-004-6853-5
15 Joseph B, Corwin JA, Li BH, et al. Cytoplasmic genetic variation and extensive cytonuclear interactions influence natural variation in the metabolome. eLife 2013; 2: e00776.
doi: 10.7554/eLife.00776
16 Kapralov MV, Filatov DA Widespread positive selection in the photosynthetic Rubisco enzyme. BMC Evolutionary Biology 2007; 7: 73.
doi: 10.1186/1471-2148-7-73
17 Koenig D, Jiménez-Gómez JM, Kimura S, et al. Comparative transcriptomics reveals patterns of selection in domesticated and wild tomato. Proceedings of the National Academy of Sciences of the United States of America 2013; 110: 28 E2655- E2662.
doi: 10.1073/pnas.1309606110
18 Lasky JR, Des Marais DL, Lowry DB, et al. Natural variation in abiotic stress responsive gene expression and local adaptation to climate in Arabidopsis thaliana . Molecular Biology and Evolution 2014; 31: 9 2283- 2296.
doi: 10.1093/molbev/msu170
19 Lee BH, Henderson DA, Zhu JK The Arabidopsis cold-responsive transcriptome and its regulation by ICE1 . The Plant Cell 2005; 17: 11 3155- 3175.
doi: 10.1105/tpc.105.035568
20 Lee BH, Lee HJ, Xiong LM, et al. A mitochondrial complex I defect impairs cold-regulated nuclear gene expression. The Plant Cell 2002; 14: 6 1235- 1251.
doi: 10.1105/tpc.010433
21 Li L, Stoeckert Jr CJ, Roos DS OrthoMCL: Identification of ortholog groups for eukaryotic genomes. Genome Research 2003; 13: 9 2178- 2189.
doi: 10.1101/gr.1224503
22 Liu TM, Tang SW, Zhu SY, et al. Transcriptome comparison reveals the patterns of selection in domesticated and wild ramie (Boehmeria nivea L^ Gaud) . Plant Molecular Biology 2014; 86: 1–2 85- 92.
doi: 10.1007/s11103-014-0214-9
23 Lovell JT, Mullen JL, Lowry DB, et al. Exploiting differential gene expression and epistasis to discover candidate genes for drought-associated QTLs in Arabidopsis thaliana . The Plant Cell 2015; 27: 4 969- 983.
doi: 10.1105/tpc.15.00122
24 Mitchell-Olds T, Schmitt J Genetic mechanisms and evolutionary significance of natural variation in Arabidopsis . Nature 2006; 441: 7096 947- 952.
doi: 10.1038/nature04878
25 Moison M, Roux F, Quadrado M, et al. Cytoplasmic phylogeny and evidence of cyto-nuclear co-adaptation in Arabidopsis thaliana . The Plant Journal 2010; 63: 5 728- 738.
doi: 10.1111/j.1365-313X.2010.04275.x
26 Niu SH, Li ZX, Yuan HW, et al. Transcriptome characterisation of Pinus tabuliformis and evolution of genes in the Pinus phylogeny . BMC Genomics 2013; 14: 263.
doi: 10.1186/1471-2164-14-263
27 Pastore D, Trono D, Laus MN, et al. Possible plant mitochondria involvement in cell adaptation to drought stress. A case study: durum wheat mitochondria. Journal of Experimental Botany 2007; 58: 2 195- 210.
doi: 10.1093/jxb/erl273
28 Provart NJ, Gil P, Chen WQ, et al. Gene expression phenotypes of Arabidopsis associated with sensitivity to low temperatures. Plant Physiology 2003; 132: 2 893- 906.
doi: 10.1104/pp.103.021261
29 Rizhsky L, Liang HJ, Shuman J, et al. When defense pathways collide. The response of Arabidopsis to a combination of drought and heat stress. Plant Physiology 2004; 134: 4 1683- 1696.
doi: 10.1104/pp.103.033431
30 Rurek M, Nuc K, Raczyńska KD, et al. Lupin nad9 and nad6 genes and their expression: 5′ termini of the nad9 gene transcripts differentiate lupin species . Gene 2003; 315: 123- 132.
doi: 10.1016/s0378-1119(03)00724-8
31 Schertl P, Braun HP Respiratory electron transfer pathways in plant mitochondria. Frontiers in Plant Science 2014; 5: 163.
doi: 10.3389/fpls.2014.00163
32 Schmid M, Davison TS, Henz SR, et al. A gene expression map of Arabidopsis thaliana development . Nature Genetics 2005; 37: 5 501- 506.
doi: 10.1038/ng1543
33 Sharma S, Villamor JG, Verslues PE Essential role of tissue-specific proline synthesis and catabolism in growth and redox balance at low water potential. Plant Physiology 2011; 157: 1 292- 304.
doi: 10.1104/pp.111.183210
34 Sloan DB Using plants to elucidate the mechanisms of cytonuclear co-evolution. New Phytologist 2015; 205: 3 1040- 1046.
doi: 10.1111/nph.12835
35 Verslues PE, Sharma S Proline metabolism and its implications for plant-environment interaction. The Arabidopsis Book 2010; 8: e0140.
doi: 10.1199/tab.0140
36 Wang LR, Zhao PS, Zhao X, et al. Physiological adaptations to osmotic stress and characterization of a polyethylene glycol-responsive gene in Braya humilis . Acta Societatis Botanicorum Poloniae 2016; 85: 1 3487.
doi: 10.5586/asbp.3487
37 Wang Y, Zhang WZ, Song LF, et al. Transcriptome analyses show changes in gene expression to accompany pollen germination and tube growth in Arabidopsis. Plant Physiology 2008; 148: 3 1201- 1211.
doi: 10.1104/pp.108.126375
38 Warwick SI, Al-Shehbaz IA, Sauder C, et al. Phylogeny of Braya and Neotorularia (Brassicaceae) based on nuclear ribosomal internal transcribed spacer and chloroplast trnL intron sequences . Canadian Journal of Botany 2004; 82: 3 376- 392.
doi: 10.1139/b04-012
39 Warwick SI, Sauder CA, Al-Shehbaz IA, et al. Phylogenetic relationships in the tribes Anchonieae, Chorisporeae, Euclidieae, and Hesperideae (Brassicaceae) based on nuclear ribosomal its DNA sequences. Annals of the Missouri Botanical Garden 2007; 94: 1 56- 78.
doi: 10.3417/0026-6493(2007)94[56:pritta]2.0.co;2
40 Winter D, Vinegar B, Nahal H, et al. An "Electronic Fluorescent Pictograph" browser for exploring and analyzing large-scale biological data sets. PLoS One 2007; 2: 8 e718.
doi: 10.1371/journal.pone.0000718
41 Wuest SE, Vijverberg K, Schmidt A, et al. Arabidopsis female gametophyte gene expression map reveals similarities between plant and animal gametes. Current Biology 2010; 20: 6 506- 512.
doi: 10.1016/j.cub.2010.01.051
42 Yang ZH PAML 4: phylogenetic analysis by maximum likelihood. Molecular Biology and Evolution 2007; 24: 8 1586- 1591.
doi: 10.1093/molbev/msm088
43 Zhang J, Xie PH, Lascoux M, et al. Rapidly evolving genes and stress adaptation of two desert poplars, Populus euphratica and P^ pruinosa . PLoS One 2013a; 8: 6 e66370.
doi: 10.1371/journal.pone.0066370
44 Zhang L, Yan HF, Wu W, et al. Comparative transcriptome analysis and marker development of two closely related Primrose species (Primula poissonii and Primula wilsonii) . BMC Genomics 2013b; 14: 329.
doi: 10.1186/1471-2164-14-329
45 Zhao PS, Wang LR, Zhao X, et al. A comparative transcriptomic analysis reveals the core genetic components of salt and osmotic stress responses in Braya humilis . PLoS One 2017; 12: 8 e0183778.
doi: 10.1371/journal.pone.0183778
46 Zheng D The system of physico-geographical regions of the Qinghai-Xizang (Tibet) Plateau. Science in China (Series D) 1996; 39: 4 410- 417.
No related articles found!
Viewed
Full text


Abstract

Cited
  Shared   
  Discussed   
[1] . [J]. Sciences in Cold and Arid Regions, 2018, 10(5): 357 -368 .
[2] . [J]. Sciences in Cold and Arid Regions, 2018, 10(5): 369 -378 .
[3] . [J]. Sciences in Cold and Arid Regions, 2018, 10(5): 413 -420 .
[4] . [J]. Sciences in Cold and Arid Regions, 2018, 10(5): 379 -391 .
[5] . [J]. Sciences in Cold and Arid Regions, 2018, 10(5): 392 -403 .
[6] . [J]. Sciences in Cold and Arid Regions, 2018, 10(5): 404 -412 .
[7] . [J]. Sciences in Cold and Arid Regions, 2018, 10(5): 421 -427 .
[8] . [J]. Sciences in Cold and Arid Regions, 2018, 10(4): 279 -285 .
[9] . [J]. Sciences in Cold and Arid Regions, 2018, 10(5): 436 -446 .
[10] . [J]. Sciences in Cold and Arid Regions, 2018, 10(4): 286 -292 .