Skip to main content
Log in

Molecular Evolution of the CPP-like Gene Family in Plants: Insights from Comparative Genomics of Arabidopsis and Rice

  • Published:
Journal of Molecular Evolution Aims and scope Submit manuscript

Abstract

CPP-like genes are members of a small family which features the existence of two similar Cys-rich domains termed CXC domains in their protein products and are distributed widely in plants and animals but do not exist in yeast. The members of this family in plants play an important role in development of reproductive tissue and control of cell division. To gain insights into how CPP-like genes evolved in plants, we conducted a comparative phylogenetic and molecular evolutionary analysis of the CPP-like gene family in Arabidopsis and rice. The results of phylogeny revealed that both gene loss and species-specific expansion contributed to the evolution of this family in Arabidopsis and rice. Both intron gain and intron loss were observed through intron/exon structure analysis for duplicated genes. Our results also suggested that positive selection was a major force during the evolution of CPP-like genes in plants, and most amino acid residues under positive selection were disproportionately located in the region outside the CXC domains. Further analysis revealed that two CXC domains and sequences connecting them might have coevolved during the long evolutionary period.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Andersen SU, Algreen-Petersen RG, Hoedl M, Jurkiewicz A, Cvitanich C, Braunschweig U, Schauser L, Oh SA, Twell D, Jensen EO (2007) The conserved cysteine-rich domain of a tesmin/TSO1-like protein binds zinc in vitro and TSO1 is required for both male and female fertility in Arabidopsis thaliana. J Exp Bot 58:3657–3670

    Article  PubMed  CAS  Google Scholar 

  • Anisimova M, Bielawski JP, Yang Z (2001) Accuracy and power of the likelihood ratio test in detecting adaptive molecular evolution. Mol Biol Evol 18:1585–1592

    PubMed  CAS  Google Scholar 

  • Initiative Arabidopsis Genome (2000) Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature 408:796–815

    Article  Google Scholar 

  • Cai J, Shin S, Wright L, Liu Y, Zhou D, Xue H, Khrebtukova I, Mattson MP, Svendsen CN, Rao MS (2006) Massively parallel signature sequencing profiling of fetal human neural precursor cells. Stem Cells Dev 15:232–244

    Article  PubMed  CAS  Google 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 Biol 4:10

    Article  PubMed  Google Scholar 

  • Cvitanich C, Pallisgaard N, Nielsen KA, Hansen AC, Larsen K, Pihakaski-Maunsbach K, Marcker KA, Jensen EO (2000) CPP1, a DNA-binding protein involved in the expression of a soybean leghemoglobin c3 gene. Proc Natl Acad Sci USA 97:8163–8168

    Article  PubMed  CAS  Google Scholar 

  • Devoto A, Hartmann HA, Piffanelli P, Elliott C, Simmons C, Taramino G, Goh CS, Cohen FE, Emerson BC, Schulze-Lefert P, Panstruga R (2003) Molecular phylogeny and evolution of the plant-specific seven-transmembrane MLO family. J Mol Evol 56:77–88

    Article  PubMed  CAS  Google Scholar 

  • Friedman R, Hughes AL (2007) Likelihood-ratio tests for positive selection of human and mouse duplicate genes reveal nonconservative and anomalous properties of widely used methods. Mol Phylogenet Evol 42:388–393

    Article  PubMed  CAS  Google Scholar 

  • Goff SA, Ricke D, Lan TH, Presting G, Wang R, Dunn M, Glazebrook J, Sessions A, Oeller P, Varma H, Hadley D, Hutchison D, Martin C, Katagiri F, Lange BM, Moughamer T, Xia Y, Budworth P, Zhong J, Miguel T, Paszkowski U, Zhang S, Colbert M, Sun WL, Chen L, Cooper B, Park S, Wood TC, Mao L, Quail P, Wing R, Dean R, Yu Y, Zharkikh A, Shen R, Sahasrabudhe S, Thomas A, Cannings R, Gutin A, Pruss D, Reid J, Tavtigian S, Mitchell J, Eldredge G, Scholl T, Miller RM, Bhatnagar S, Adey N, Rubano T, Tusneem N, Robinson R, Feldhaus J, Macalma T, Oliphant A, Briggs S (2002) A draft sequence of the rice genome (Oryza sativa L. ssp. japonica). Science 296:92–100

    Article  PubMed  CAS  Google Scholar 

  • Goh CS, Bogan AA, Joachimiak M, Walther D, Cohen FE (2000) Co-evolution of proteins with their interaction partners. J Mol Biol 299:283–293

    Article  PubMed  CAS  Google Scholar 

  • Hauser BA, He JQ, Park SO, Gasser CS (2000) TSO1 is a novel protein that modulates cytokinesis and cell expansion in Arabidopsis. Development 127:2219–2226

    PubMed  CAS  Google Scholar 

  • Hauser BA, Villanueva JM, Gasser CS (1998) Arabidopsis TSO1 regulates directional processes in cells during floral organogenesis. Genetics 150:411–423

    PubMed  CAS  Google Scholar 

  • International Rice Genome Sequencing Project (2005) The map-based sequence of the rice genome. Nature 436:793–800

    Article  Google Scholar 

  • Jain M, Tyagi AK, Khurana JP (2006) Genome-wide analysis, evolutionary expansion, and expression of early auxin-responsive SAUR gene family in rice (Oryza sativa). Genomics 88:360–371

    Article  PubMed  CAS  Google Scholar 

  • Jia L, Clegg MT, Jiang T (2004) Evolutionary dynamics of the DNA-binding domains in putative R2R3-MYB genes identified from rice subspecies indica and japonica genomes. Plant Physiol 134:575–585

    Article  PubMed  CAS  Google Scholar 

  • Jordan IK, Makarova KS, Spouge JL, Wolf YI, Koonin EV (2001) Lineage-specific gene expansions in bacterial and archaeal genomes. Genome Res 11:555–565

    Article  PubMed  CAS  Google Scholar 

  • Kong H, Landherr LL, Frohlich MW, Leebens-Mack J, Ma H, dePamphilis CW (2007) Patterns of gene duplication in the plant SKP1 gene family in angiosperms: evidence for multiple mechanisms of rapid gene birth. Plant J 50:873–885

    Article  PubMed  CAS  Google Scholar 

  • Lespinet O, Wolf YI, Koonin EV, Aravind L (2002) The role of lineage-specific gene family expansion in the evolution of eukaryotes. Genome Res 12:1048–1059

    Article  PubMed  CAS  Google Scholar 

  • Liu Q, Xue Q (2007) Molecular phylogeny, evolution, and functional divergence of the LSD1-like gene family: inference from the rice genome. J Mol Evol 64:354–363

    Article  PubMed  CAS  Google Scholar 

  • Maher C, Stein L, Ware D (2006) Evolution of Arabidopsis microRNA families through duplication events. Genome Res 16:510–519

    Article  PubMed  CAS  Google Scholar 

  • Martinez-Castilla LP, Alvarez-Buylla ER (2003) Adaptive evolution in the Arabidopsis MADS-box gene family inferred from its complete resolved phylogeny. Proc Natl Acad Sci USA 100:13407–13412

    Article  PubMed  CAS  Google Scholar 

  • Mondragon-Palomino M, Gaut BS (2005) Gene conversion and the evolution of three leucine-rich repeat gene families in Arabidopsis thaliana. Mol Biol Evol 22:2444–2456

    Article  PubMed  CAS  Google Scholar 

  • Mondragon-Palomino M, Meyers BC, Michelmore RW, Gaut BS (2002) Patterns of positive selection in the complete NBS-LRR gene family of Arabidopsis thaliana. Genome Res 12:1305–1315

    Article  PubMed  CAS  Google Scholar 

  • Pazos F, Valencia A (2001) Similarity of phylogenetic trees as indicator of protein-protein interaction. Protein Eng 14:609–614

    Article  PubMed  CAS  Google Scholar 

  • Raes J, Vandepoele K, Simillion C, Saeys Y, Van de Peer Y (2003) Investigating ancient duplication events in the Arabidopsis genome. J Struct Funct Genomics 3:117–129

    Article  PubMed  CAS  Google Scholar 

  • Riechmann JL, Heard J, Martin G, Reuber L, Jiang C, Keddie J, Adam L, Pineda O, Ratcliffe OJ, Samaha RR, Creelman R, Pilgrim M, Broun P, Zhang JZ, Ghandehari D, Sherman BK, Yu G (2000) Arabidopsis transcription factors: genome-wide comparative analysis among eukaryotes. Science 290:2105–2110

    Article  PubMed  CAS  Google Scholar 

  • Schauser L, Wieloch W, Stougaard J (2005) Evolution of NIN-like proteins in Arabidopsis, rice, and Lotus japonicus. J Mol Evol 60:229–237

    Article  PubMed  CAS  Google Scholar 

  • Shiu SH, Bleecker AB (2003) Expansion of the receptor-like kinase/Pelle gene family and receptor-like proteins in Arabidopsis. Plant Physiol 132:530–543

    Article  PubMed  CAS  Google Scholar 

  • Shiu SH, Karlowski WM, Pan R, Tzeng YH, Mayer KF, Li WH (2004) Comparative analysis of the receptor-like kinase family in Arabidopsis and rice. Plant Cell 16:1220–1234

    Article  PubMed  CAS  Google Scholar 

  • Simillion C, Vandepoele K, Van Montagu MC, Zabeau M, Van de Peer Y (2002) The hidden duplication past of Arabidopsis thaliana. Proc Natl Acad Sci USA 99:13627–13632

    Article  PubMed  CAS  Google Scholar 

  • Song JY, Leung T, Ehler LK, Wang C, Liu Z (2000) Regulation of meristem organization and cell division by TSO1, an Arabidopsis gene with cysteine-rich repeats. Development 127:2207–2217

    PubMed  CAS  Google Scholar 

  • Sonnhammer EL, Eddy SR, Durbin R (1997) Pfam: a comprehensive database of protein domain families based on seed alignments. Proteins 28:405–420

    Article  PubMed  CAS  Google Scholar 

  • Sun X, Cao Y, Wang S (2006) Point mutations with positive selection were a major force during the evolution of a receptor-kinase resistance gene family of rice. Plant Physiol 140:998–1008

    Article  PubMed  CAS  Google Scholar 

  • Suyama M, Torrents D, Bork P (2006) PAL2NAL: robust conversion of protein sequence alignments into the corresponding codon alignments. Nucleic Acids Res 34:W609–612

    Article  PubMed  CAS  Google Scholar 

  • Swanson WJ, Yang Z, Wolfner MF, Aquadro CF (2001) Positive Darwinian selection drives the evolution of several female reproductive proteins in mammals. Proc Natl Acad Sci USA 98:2509–2514

    Article  PubMed  CAS  Google Scholar 

  • Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol Biol Evol 24:1596–1599

    Article  PubMed  CAS  Google Scholar 

  • Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25:4876–4882

    Article  PubMed  CAS  Google Scholar 

  • Wang C, Liu Z (2006) Arabidopsis ribonucleotide reductases are critical for cell cycle progression, DNA damage repair, and plant development. Plant Cell 18:350–365

    Article  PubMed  CAS  Google Scholar 

  • Wang X, Shi X, Hao B, Ge S, Luo J (2005) Duplication and DNA segmental loss in the rice genome: implications for diploidization. New Phytol 165:937–946

    Article  PubMed  CAS  Google Scholar 

  • Xiong Y, Liu T, Tian C, Sun S, Li J, Chen M (2005) Transcription factors in rice: a genome-wide comparative analysis between monocots and eudicots. Plant Mol Biol 59:191–203

    Article  PubMed  CAS  Google Scholar 

  • Yang X, Tuskan GA, Cheng MZ (2006) Divergence of the Dof gene families in poplar, Arabidopsis, and rice suggests multiple modes of gene evolution after duplication. Plant Physiol 142:820–830

    Article  PubMed  CAS  Google Scholar 

  • Yang Z (2007) PAML 4: phylogenetic analysis by maximum likelihood. Mol Biol Evol 24:1586–1591

    Article  PubMed  CAS  Google Scholar 

  • Yang Z, Nielsen R, Goldman N, Pedersen AM (2000) Codon-substitution models for heterogeneous selection pressure at amino acid sites. Genetics 155:431–449

    PubMed  CAS  Google Scholar 

  • Yang Z, Wong WS, Nielsen R (2005) Bayes empirical bayes inference of amino acid sites under positive selection. Mol Biol Evol 22:1107–1118

    Article  PubMed  CAS  Google Scholar 

  • Yang Z, Wang X, Gu S, Hu Z, Xu H, Xu C (2008) Comparative study of SBP-box gene family in Arabidopsis and rice. Gene 407:1–11

    Article  PubMed  CAS  Google Scholar 

  • Yu J, Hu S, Wang J, Wong GK, Li S, Liu B, Deng Y, Dai L, Zhou Y, Zhang X, Cao M, Liu J, Sun J, Tang J, Chen Y, Huang X, Lin W, Ye C, Tong W, Cong L, Geng J, Han Y, Li L, Li W, Hu G, Huang X, Li W, Li J, Liu Z, Li L, Liu J, Qi Q, Liu J, Li L, Li T, Wang X, Lu H, Wu T, Zhu M, Ni P, Han H, Dong W, Ren X, Feng X, Cui P, Li X, Wang H, Xu X, Zhai W, Xu Z, Zhang J, He S, Zhang J, Xu J, Zhang K, Zheng X, Dong J, Zeng W, Tao L, Ye J, Tan J, Ren X, Chen X, He J, Liu D, Tian W, Tian C, Xia H, Bao Q, Li G, Gao H, Cao T, Wang J, Zhao W, Li P, Chen W, Wang X, Zhang Y, Hu J, Wang J, Liu S, Yang J, Zhang G, Xiong Y, Li Z, Mao L, Zhou C, Zhu Z, Chen R, Hao B, Zheng W, Chen S, Guo W, Li G, Liu S, Tao M, Wang J, Zhu L, Yuan L, Yang H (2002) A draft sequence of the rice genome (Oryza sativa L. ssp. indica). Science 296:79–92

    Article  PubMed  CAS  Google Scholar 

  • Yu J, Wang J, Lin W et al (2005) The genomes of Oryza sativa: a history of duplications. PLoS Biol 3:e38

    Article  PubMed  Google Scholar 

  • Zhang S, Chen C, Li L, Meng L, Singh J, Jiang N, Deng XW, He ZH, Lemaux PG (2005) Evolutionary expansion, gene structure, and expression of the rice wall-associated kinase gene family. Plant Physiol 139:1107–1124

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

The authors are grateful to Professor Kreitman for the helpful comments and criticisms. This work was supported by the National Basic Research Program of China (Grant 2006CB101700), the National High-Tech R&D Program (Grant 2006AA10Z165), the Program for New Century Excellent Talents in University (Grant NCET-05-0502), and the Program for Innovative Research of Graduate Students in Jiangsu Province (Grant CX07B-186z).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Chenwu Xu.

Additional information

Zefeng Yang and Shiliang Gu contributed equally to this work.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Yang, Z., Gu, S., Wang, X. et al. Molecular Evolution of the CPP-like Gene Family in Plants: Insights from Comparative Genomics of Arabidopsis and Rice. J Mol Evol 67, 266–277 (2008). https://doi.org/10.1007/s00239-008-9143-z

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00239-008-9143-z

Keywords

Navigation