Planta

, Volume 230, Issue 1, pp 149–163 | Cite as

Genome-wide identification of BURP domain-containing genes in rice reveals a gene family with diverse structures and responses to abiotic stresses

Original Article

Abstract

Increasing evidence suggests that a gene family encoding proteins containing BURP domains have diverse functions in plants, but systematic characterization of this gene family have not been reported. In this study, 17 BURP family genes (OsBURP0117) were identified and analyzed in rice (Oryza sativa L.). These genes have diverse exon–intron structures and distinct organization of putative motifs. Based on the phylogenetic analysis of BURP protein sequences from rice and other plant species, the BURP family was classified into seven subfamilies, including two subfamilies (BURP V and BURP VI) with members from rice only and one subfamily (BURP VII) with members from monocotyledons only. Two BURP gene clusters, belonging to BURP V and BURP VI, were located in the duplicated region on chromosome 5 and 6 of rice, respectively. Transcript level analysis of BURP genes of rice in various tissues and organs revealed different tempo-spatial expression patterns, suggesting that these genes may function at different stages of plant growth and development. Interestingly, all the genes of the BURP VII subfamily were predominantly expressed in flower organs. We also investigated the expression patterns of BURP genes of rice under different stress conditions. The results suggested that, except for two genes (OsBURP01 and OsBURP13), all other members were induced by at least one of the stresses including drought, salt, cold, and abscisic acid treatment. Two genes (OsBURP05 and OsBURP16) were responsive to all the stress treatments and most of the OsBURP genes were responsive to salt stress. Promoter sequence analysis revealed an over-abundance of stress-related cis-elements in the stress-responsive genes. The data presented here provide important clues for elucidating the functions of genes of this family.

Keywords

Abiotic stress BURP domain Oryza RD22 Transcript level 

Abbreviations

ABA

Abscisic acid

ABRE

ABA responsive element

BURP

BNM2, USP, RD22, and PG1β

DRE

Dehydration-responsive element

LTRE

Low temperature-responsive element

Notes

Acknowledgments

This work was supported by the grants from the National Program on the Development of Basic Research, the National Program on High Technology Development, the National Natural Science Foundation, and the Ministry of Education of China.

Supplementary material

425_2009_929_MOESM1_ESM.doc (51 kb)
Supplementary material 1 (DOC 51 kb)

References

  1. Abe H, Yamaguchi-Shinozaki K, Urao T, Iwasaki T, Hosokawa D, Shinozaki K (1997) Role of Arabidopsis MYC and MYB homologs in drought- and abscisic acid-regulated gene expression. Plant Cell 9:1859–1868PubMedCrossRefGoogle Scholar
  2. Abe H, Urao T, Ito T, Seki M, Shinozaki K, Yamaguchi-Shinozaki K (2003) Arabidopsis AtMYC2 (bHLH) and AtMYB2 (MYB) function as transcriptional activators in abscisic acid signaling. Plant Cell 15:63–78PubMedCrossRefGoogle Scholar
  3. Bailey TL, Williams N, Misleh C, Li WW (2006) MEME: discovering and analyzing DNA and protein sequence motifs. Nucleic Acids Res 34:W369–W373PubMedCrossRefGoogle Scholar
  4. Banzai T, Sumiya K, Hanagata N, Dubinsky Z, Karube I (2002) Molecular cloning and characterization of genes encoding BURP domain-containing protein in the mangrove, Bruguiera gymnorrhiza. Trees 16:87–93CrossRefGoogle Scholar
  5. Bassüner R, Bäumlein H, Huth A, Jung R, Wobus U, Rapoport TA, Saalbach G, Müntz K (1988) Abundant embryonic mRNA in field bean (Vicia faba L.) codes for a new class of seed proteins: cDNA cloning and characterization of the primary translation product. Plant Mol Biol 11:321–334CrossRefGoogle Scholar
  6. Batchelor AK, Boutilier K, Miller SS, Hattori J, Bowman LA, Hu M, Lantin S, Johnson DA, Miki BL (2002) SCB1, a BURP-domain protein gene, from developing soybean seed coats. Planta 215:523–532PubMedCrossRefGoogle Scholar
  7. Baumlein H, Boerjan W, Nagy I, Bassuner R, Van Montagu M, Inze D, Wobus U (1991) A novel seed protein gene from Vicia faba is developmentally regulated in transgenic tobacco and Arabidopsis plants. Mol Gen Genet 225:459–467PubMedCrossRefGoogle Scholar
  8. Boutilier KA, Gines MJ, DeMoor JM, Huang B, Baszczynski CL, Iyer VN, Miki BL (1994) Expression of the BnmNAP subfamily of napin genes coincides with the induction of Brassica microspore embryogenesis. Plant Mol Biol 26:1711–1723PubMedCrossRefGoogle Scholar
  9. Chen L, Guan L, Seo M, Hoffmann F, Adachi T (2005) Developmental expression of ASG-1 during gametogenesis in apomictic guinea grass (Panicum maximum). J Plant Physiol 162:1141–1148PubMedCrossRefGoogle Scholar
  10. Datta N, LaFayette PR, Kroner PA, Nagao RT, Key JL (1993) Isolation and characterization of three families of auxin down-regulated cDNA clones. Plant Mol Biol 21:859–869PubMedCrossRefGoogle Scholar
  11. Finn RD, Mistry J, Schuster-Bockler B, Griffiths-Jones S, Hollich V, Lassmann T, Moxon S, Marshall M, Khanna A, Durbin R, Eddy SR, Sonnhammer EL, Bateman A (2006) Pfam: clans, web tools and services. Nucleic Acids Res 34:D247–D251PubMedCrossRefGoogle Scholar
  12. Garcia-Hernandez M, Berardini TZ, Chen G, Crist D, Doyle A, Huala E, Knee E, Lambrecht M, Miller N, Mueller LA, Mundodi S, Reiser L, Rhee SY, Scholl R, Tacklind J, Weems DC, Wu Y, Xu I, Yoo D, Yoon J, Zhang P (2002) TAIR: a resource for integrated Arabidopsis data. Funct Integr Genomics 2:239–253PubMedCrossRefGoogle Scholar
  13. Granger C, Coryell V, Khanna A, Keim P, Vodkin L, Shoemaker RC (2002) Identification, structure, and differential expression of members of a BURP domain containing protein family in soybean. Genome 45:693–701PubMedCrossRefGoogle Scholar
  14. Hattori J, Boutilier KA, van Lookeren Campagne MM, Miki BL (1998) A conserved BURP domain defines a novel group of plant proteins with unusual primary structures. Mol Gen Genet 259:424–428PubMedCrossRefGoogle Scholar
  15. Higo K, Ugawa Y, Iwamoto M, Korenaga T (1999) Plant cis-acting regulatory DNA elements (PLACE) database: 1999. Nucleic Acids Res 27:297–300PubMedCrossRefGoogle Scholar
  16. Jeon JS, Chung YY, Lee S, Yi GH, Oh BG, An G (1999) Isolation and characterization of an anther-specific gene, RA8, from rice (Oryza sativa L.). Plant Mol Biol 39:35–44PubMedCrossRefGoogle Scholar
  17. Kumar S, Tamura K, Nei M (2004) MEGA3: Integrated software for molecular evolutionary genetics analysis and sequence alignment. Brief Bioinform 5:150–163PubMedCrossRefGoogle Scholar
  18. Letunic I, Copley RR, Schmidt S, Ciccarelli FD, Doerks T, Schultz J, Ponting CP, Bork P (2004) SMART 4.0: towards genomic data integration. Nucleic Acids Res 32:D142–D144PubMedCrossRefGoogle Scholar
  19. Liang D, Wu C, Li C, Xu C, Zhang J, Kilian A, Li X, Zhang Q, Xiong L (2006) Establishment of a patterned GAL4-VP16 transactivation system for discovering gene function in rice. Plant J 46:1059–1072PubMedCrossRefGoogle Scholar
  20. Mulder NJ, Apweiler R (2008) The InterPro database and tools for protein domain analysis. In: Current Protocols Bioinformatics, chap 2, Unit 2.7. Wiley, New YorkGoogle Scholar
  21. Narusaka Y, Nakashima K, Shinwari ZK, Sakuma Y, Furihata T, Abe H, Narusaka M, Shinozaki K, Yamaguchi-Shinozaki K (2003) Interaction between two cis-acting elements, ABRE and DRE, in ABA-dependent expression of Arabidopsis rd29A gene in response to dehydration and high-salinity stresses. Plant J 34:137–148PubMedCrossRefGoogle Scholar
  22. Ouyang S, Zhu W, Hamilton J, Lin H, Campbell M, Childs K, Thibaud-Nissen F, Malek RL, Lee Y, Zheng L, Orvis J, Haas B, Wortman J, Buell CR (2007) The TIGR rice genome annotation resource: improvements and new features. Nucleic Acids Res 35:D883–D887PubMedCrossRefGoogle Scholar
  23. Pla M, Vilardell J, Guiltinan MJ, Marcotte WR, Niogret MF, Quatrano RS, Pages M (1993) The cis-regulatory element CCACGTGG is involved in ABA and water-stress responses of the maize gene rab28. Plant Mol Biol 21:259–266PubMedCrossRefGoogle Scholar
  24. Ragland M, Soliman KM (1997) Sali5-4a and Sali3-2, two genes induced by aluminum in soybean roots. Plant Physiol 114:395CrossRefGoogle Scholar
  25. Ramakers C, Ruijter JM, Deprez RH, Moorman AF (2003) Assumption-free analysis of quantitative real-time polymerase chain reaction (PCR) data. Neurosci Lett 339:62–66PubMedCrossRefGoogle Scholar
  26. Rensing SA, Lang D, Zimmer AD, Terry A, Salamov A, Shapiro H, Nishiyama T, Perroud PF, Lindquist EA, Kamisugi Y, Tanahashi T, Sakakibara K, Fujita T, Oishi K, Shin IT, Kuroki Y, Toyoda A, Suzuki Y, Hashimoto S, Yamaguchi K, Sugano S, Kohara Y, Fujiyama A, Anterola A, Aoki S, Ashton N, Barbazuk WB, Barker E, Bennetzen JL, Blankenship R, Cho SH, Dutcher SK, Estelle M, Fawcett JA, Gundlach H, Hanada K, Heyl A, Hicks KA, Hughes J, Lohr M, Mayer K, Melkozernov A, Murata T, Nelson DR, Pils B, Prigge M, Reiss B, Renner T, Rombauts S, Rushton PJ, Sanderfoot A, Schween G, Shiu SH, Stueber K, Theodoulou FL, Tu H, Van de Peer Y, Verrier PJ, Waters E, Wood A, Yang L, Cove D, Cuming AC, Hasebe M, Lucas S, Mishler BD, Reski R, Grigoriev IV, Quatrano RS, Boore JL (2008) The Physcomitrella genome reveals evolutionary insights into the conquest of land by plants. Science 319:64–69PubMedCrossRefGoogle Scholar
  27. Retief JD (2000) Phylogenetic analysis using PHYLIP. Methods Mol Biol 132:243–258PubMedGoogle Scholar
  28. Tang Y-L, Li X-J, Zhong Y-T, Zhang Y-Z (2007) Functional analysis of soybean SALI3-2 in yeast. J Shenzhen Univ Sci Eng 24:324–330Google Scholar
  29. 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 25:4876–4882PubMedCrossRefGoogle Scholar
  30. Treacy BK, Hattori J, Prud’homme I, Barbour E, Boutilier K, Baszczynski CL, Huang B, Johnson DA, Miki BL (1997) Bnm1, a Brassica pollen-specific gene. Plant Mol Biol 34:603–611PubMedCrossRefGoogle Scholar
  31. Wang A, Xia Q, Xie W, Datla R, Selvaraj G (2003) The classical Ubisch bodies carry a sporophytically produced structural protein (RAFTIN) that is essential for pollen development. Proc Natl Acad Sci USA 100:14487–14492PubMedCrossRefGoogle Scholar
  32. Ware D (2007) Gramene: a resource for comparative grass genomics. Methods Mol Biol 406:315–330PubMedCrossRefGoogle Scholar
  33. Watson CF, Zheng L, DellaPenna D (1994) Reduction of tomato polygalacturonase beta subunit expression affects pectin solubilization and degradation during fruit ripening. Plant Cell 6:1623–1634PubMedCrossRefGoogle Scholar
  34. Xiong L, Yang Y (2003) Disease resistance and abiotic stress tolerance in rice are inversely modulated by an abscisic acid-inducible mitogen-activated protein kinase. Plant Cell 15:745–759PubMedCrossRefGoogle Scholar
  35. Yamaguchi-Shinozaki K, Shinozaki K (1993) The plant hormone abscisic acid mediates the drought-induced expression but not the seed-specific expression of rd22, a gene responsive to dehydration stress in Arabidopsis thaliana. Mol Gen Genet 238:17–25PubMedGoogle Scholar
  36. Yamaguchi-Shinozaki K, Shinozaki K (1994) A novel cis-acting element in an Arabidopsis gene is involved in responsiveness to drought, low-temperature, or high-salt stress. Plant Cell 6:251–264PubMedCrossRefGoogle Scholar
  37. Yamaguchi-Shinozaki K, Shinozaki K (2005) Organization of cis-acting regulatory elements in osmotic- and cold-stress-responsive promoters. Trends Plant Sci 10:88–94PubMedCrossRefGoogle Scholar
  38. Yu S, Zhang L, Zuo K, Li Z, Tang K (2004) Isolation and characterization of a BURP domain-containing gene BnBDC1 from Brassica napus involved in abiotic and biotic stress. Physiol Plant 122:210–218CrossRefGoogle Scholar
  39. Zheng L, Heupel RC, DellaPenna D (1992) The beta subunit of tomato fruit polygalacturonase isoenzyme 1: isolation, characterization, and identification of unique structural features. Plant Cell 4:1147–1156PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2009

Authors and Affiliations

  • Xipeng Ding
    • 1
  • Xin Hou
    • 1
  • Kabin Xie
    • 1
  • Lizhong Xiong
    • 1
    • 2
  1. 1.National Key Laboratory of Crop Genetic Improvement, National Center of Plant Gene Research (Wuhan)Huazhong Agricultural UniversityWuhanChina
  2. 2.National Key Laboratory of Crop Genetic ImprovementHuazhong Agricultural UniversityWuhanChina

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