Molecular Genetics and Genomics

, Volume 283, Issue 4, pp 381–396

RNase T2 genes from rice and the evolution of secretory ribonucleases in plants

  • Gustavo C. MacIntosh
  • Melissa S. Hillwig
  • Alexander Meyer
  • Lex Flagel
Original Paper

Abstract

The plant RNase T2 family is divided into two different subfamilies. S-RNases are involved in rejection of self-pollen during the establishment of self-incompatibility in three plant families. S-like RNases, on the other hand, are not involved in self-incompatibility, and although gene expression studies point to a role in plant defense and phosphate recycling, their biological roles are less well understood. Although S-RNases have been subjects of many phylogenetic studies, few have included an extensive analysis of S-like RNases, and genome-wide analyses to determine the number of S-like RNases in fully sequenced plant genomes are missing. We characterized the eight RNase T2 genes present in the Oryza sativa genome; and we also identified the full complement of RNase T2 genes present in other fully sequenced plant genomes. Phylogenetics and gene expression analyses identified two classes among the S-like RNase subfamily. Class I genes show tissue specificity and stress regulation. Inactivation of RNase activity has occurred repeatedly throughout evolution. On the other hand, Class II seems to have conserved more ancestral characteristics; and, unlike other S-like RNases, genes in this class are conserved in all plant species analyzed and most are constitutively expressed. Our results suggest that gene duplication resulted in high diversification of Class I genes. Many of these genes are differentially expressed in response to stress, and we propose that protein characteristics, such as the increase in basic residues can have a defense role independent of RNase activity. On the other hand, constitutive expression and phylogenetic conservation suggest that Class II S-like RNases may have a housekeeping role.

Keywords

S-like RNases Evolution Rice Housekeeping Inactive RNase 

Supplementary material

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References

  1. Acquati F, Possati L et al (2005) Tumor and metastasis suppression by the human RNASET2 gene. Int J Oncol 26(5):1159–1168PubMedGoogle Scholar
  2. Altschul SF, Gish W et al (1990) Basic local alignment search tool. J Mol Biol 215(3):403–410PubMedGoogle Scholar
  3. Banks JA (2009) Selaginella and 400 million years of separation. Ann Rev Plant Biol 60(1):223–238. doi:10.1146/annurev.arplant.59.032607.092851 CrossRefGoogle Scholar
  4. Bariola P, Green P (1997) Plant ribonucleases. In: D’Alessio G, Riordan J (eds) Ribonucleases: structures and functions. Academic Press, New York, pp 163–190Google Scholar
  5. Bariola PA, Howard CJ et al (1994) The Arabidopsis ribonuclease gene Rns1 is tightly controlled in response to phosphate limitation. Plant J 6(5):673–685CrossRefPubMedGoogle Scholar
  6. Bariola PA, MacIntosh GC et al (1999) Regulation of S-like ribonuclease levels in arabidopsis: antisense inhibition of RNS1 or RNS2 elevates anthocyanin accumulation. Plant Physiol 119(1):331–342CrossRefPubMedGoogle Scholar
  7. Bodenhausen N, Reymond P (2007) Signaling pathways controlling induced resistance to insect herbivores in Arabidopsis. Mol Plant Microbe Interact 20(11):1406–1420. doi:10.1094/Mpmi-20-11-1406 CrossRefPubMedGoogle Scholar
  8. Boix E, Nogues MV (2007) Mammalian antimicrobial proteins and peptides: overview on the RNase A superfamily members involved in innate host defence. Mol Biosyst 3(5):317–335. doi:10.1039/B617527a CrossRefPubMedGoogle Scholar
  9. Campomenosi P, Salis S et al (2006) Characterization of RNASET2, the first human member of the Rh/T2/S family of glycoproteins. Arch Biochem Biophys 449(1–2):17–26. doi:10.1016/j.abb.2006.02.022 CrossRefPubMedGoogle Scholar
  10. Carreras E, Boix E et al (2003) Both aromatic and cationic residues contribute to the membrane-lytic and bactericidal activity of eosinophil cationic protein. Biochemistry 42(22):6636–6644. doi:10.1021/bi0273011 CrossRefPubMedGoogle Scholar
  11. Carter C, Pan S et al (2004) The vegetative vacuole proteome of Arabidopsis thaliana reveals predicted and unexpected proteins. Plant Cell 16(12):3285–3303. doi:10.1105/tpc.104.027078 CrossRefPubMedGoogle Scholar
  12. Chang SH, Ying H et al (2003) Expression of a wheat S-like RNase (WRN1) cDNA during natural- and dark-induced senescence. Acta Bot Sin 45(9):1071–1075Google Scholar
  13. Cheng LJ, Wang F et al (2007) Mutation in nicotinamide aminotransferase stimulated the Fe(II) acquisition system and led to iron accumulation in rice. Plant Physiol 145(4):1647–1657. doi:10.1104/pp.107.107912 CrossRefPubMedGoogle Scholar
  14. Cho S, Zhang JZ (2007) Zebrafish ribonucleases are bactericidal: Implications for the origin of the vertebrate RNase a superfamily. Mol Biol Evol 24(5):1259–1268. doi:10.1093/molbev/msm047 CrossRefPubMedGoogle Scholar
  15. Clarke AE, Newbigin E (1993) Molecular aspects of self-incompatibility in flowering plants. Ann Rev Genet 27(1):257CrossRefPubMedGoogle Scholar
  16. Condon C, Putzer H (2002) The phylogenetic distribution of bacterial ribonucleases. Nucleic Acids Res 30(24):5339–5346CrossRefPubMedGoogle Scholar
  17. Cruz-Garcia F, Hancock CN et al (2003) S-RNase complexes and pollen rejection. J Exp Bot 54(380):123–130. doi:10.1093/jxb/erg045 CrossRefPubMedGoogle Scholar
  18. Derelle E, Ferraz C et al (2006) Genome analysis of the smallest free-living eukaryote Ostreococcus tauri unveils many unique features. Proc Natl Acad Sci USA 103(31):11647–11652. doi:10.1073/pnas.0604795103 CrossRefPubMedGoogle Scholar
  19. Deshpande RA, Shankar V (2002) Ribonucleases from T2 family. Crit Rev Microbiol 28(2):79–122. doi:10.1080/1040-840291046704 CrossRefPubMedGoogle Scholar
  20. Emanuelsson O, Brunak S et al (2007) Locating proteins in the cell using TargetP, SignalP and related tools. Nat Protoc 2(4):953–971. doi:10.1038/nprot.2007.131 CrossRefPubMedGoogle Scholar
  21. Galiana E, Bonnet P et al (1997) RNase activity prevents the growth of a fungal pathogen in tobacco leaves and increases upon induction of systemic acquired resistance with elicitin. Plant Physiol 115(4):1557–1567CrossRefPubMedGoogle Scholar
  22. Gan JR, Yu L et al (2004) The three-dimensional structure and X-ray sequence reveal that trichomaglin is a novel S-like ribonuclease. Structure 12(6):1015–1025. doi:10.1016/j.str.2004.03.023 CrossRefPubMedGoogle Scholar
  23. Gasteiger E, Hoogland C (2005) Protein identification and analysis tools on the ExPASy server. In: Walker JM et al (eds) The proteomics protocols handbook. Humana Press, Totowa, pp 571–607CrossRefGoogle Scholar
  24. Gausing K (2000) A barley gene (rsh1) encoding a ribonuclease S-like homologue specifically expressed in young light-grown leaves. Planta 210(4):574–579CrossRefPubMedGoogle Scholar
  25. Green PJ (1994) The ribonucleases of higher plants. Annu Rev Plant Phys 45:421–445CrossRefGoogle Scholar
  26. Gross N, Wasternack C et al (2004) Wound-induced RNaseLE expression is jasmonate and systemin independent and occurs only locally in tomato (Lycopersicon esculentum cv. Lukullus). Phytochemistry 65(10):1343–1350. doi:10.1016/j.phytochem.2004.04.036
  27. Hillwig MS, Lebrasseur ND et al (2008) Impact of transcriptional, ABA-dependent, and ABA-independent pathways on wounding regulation of RNS1 expression. Mol Genet Genomics 280(3):249–261. doi:10.1007/s00438-008-0360-3 CrossRefPubMedGoogle Scholar
  28. Hillwig MS, Rizhsky L et al (2009) Zebrafish RNase T2 genes and the evolution of secretory ribonucleases in animals. BMC Evol Biol 9(1):170. doi:10.1186/1471-2148-9-170
  29. Hirose N, Makita N et al (2007) Overexpression of a type-A response regulator alters rice morphology and cytokinin metabolism. Plant Cell Physiol 48(3):523–539. doi:10.1093/pcp/pcm022 CrossRefPubMedGoogle Scholar
  30. Hiscock SJ, Kues U et al (1996) Molecular mechanisms of self-incompatibility in flowering plants and fungi—different means to the same end. Trends Cell Biol 6(11):421–428. doi:S0962-8924(96)10037-4[pii] CrossRefPubMedGoogle Scholar
  31. Horton P, Park KJ et al (2007) WoLF PSORT: protein localization predictor. Nucleic Acids Res 35:W585–W587. doi:10.1093/Nar/Gkm259 CrossRefPubMedGoogle Scholar
  32. Hua ZH, Fields A et al (2008) Biochemical models for S-RNase based self-incompatibility. Mol Plant 1(4):575–585CrossRefPubMedGoogle Scholar
  33. Huang YC, Lin YM et al (2007) The flexible and clustered lysine residues of human ribonuclease 7 are critical for membrane permeability and antimicrobial activity. J Biol Chem 282(7):4626–4633. doi:10.1074/jbc.M607321200 CrossRefPubMedGoogle Scholar
  34. Huelsenbeck JP, Ronquist F (2001) MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 17(8):754–755CrossRefPubMedGoogle Scholar
  35. Hugot K, Ponchet M et al (2002) A tobacco S-like RNase inhibits hyphal elongation of plant pathogens. Mol Plant Microbe Interact 15(3):243–250CrossRefPubMedGoogle Scholar
  36. Igic B, Kohn JR (2001) Evolutionary relationships among self-incompatibility RNases. Proc Natl Acad Sci USA 98(23):13167–13171CrossRefPubMedGoogle Scholar
  37. International Rice Genome Sequencing Project (2005) The map-based sequence of the rice genome. Nature 436(7052):793–800. doi:http://www.nature.com/nature/journal/v436/n7052/suppinfo/nature03895_S1.html Google Scholar
  38. Irie M (1999) Structure-function relationships of acid ribonucleases: lysosomal, vacuolar, and periplasmic enzymes. Pharmacol Ther 81(2):77–89 S0163-7258(98)00035-7[pii]CrossRefPubMedGoogle Scholar
  39. Iwama M, Ogawa Y et al (2001) Amino acid sequence and characterization of a rice bran ribonuclease. Biol Pharm Bull 24(7):760–766CrossRefPubMedGoogle Scholar
  40. Kariu T, Sano K et al (1998) Isolation and characterization of a wound-inducible ribonuclease from Nicotiana glutinosa leaves. Biosci Biotech Biochem 62(6):1144–1151CrossRefGoogle Scholar
  41. Kock M, Theierl K et al (1998) Extracellular administration of phosphate-sequestering metabolites induces ribonucleases in cultured tomato cells. Planta 204(3):404–407CrossRefGoogle Scholar
  42. Kurata N, Kariu T et al (2002) Molecular cloning of cDNAs encoding ribonuclease-related proteins in Nicotiana glutinosa leaves, as induced in response to wounding or to TMV-infection. Biosci Biotech Biochem 66(2):391–397CrossRefGoogle Scholar
  43. Lawton-Rauh A (2003) Evolutionary dynamics of duplicated genes in plants. Mol Phylogenet Evol 29(3):396–409. doi:10.1016/j.ympev.2003.07.004 CrossRefPubMedGoogle Scholar
  44. LeBrasseur ND, MacIntosh GC et al (2002) Local and systemic wound-induction of RNase and nuclease activities in Arabidopsis: RNS1 as a marker for a JA-independent systemic signaling pathway. Plant J 29(4):393–403CrossRefPubMedGoogle Scholar
  45. Lers A, Khalchitski A et al (1998) Senescence-induced RNases in tomato. Plant Mol Biol 36(3):439–449CrossRefPubMedGoogle Scholar
  46. Lers A, Sonego L et al (2006) Suppression of LX ribonuclease in tomato results in a delay of leaf senescence and abscission. Plant Physiol 142(2):710–721. doi:10.1104/pp.106.080135 CrossRefPubMedGoogle Scholar
  47. Liang L, Lai Z et al (2002) AhSL28, a senescence and phosphate starvation-induced S-like RNase gene in Antirrhinum. Biochim Biophys Acta 1579(1):64–71. doi:S0167478102005079[pii] PubMedGoogle Scholar
  48. MacIntosh GC, Bariola PA et al (2001) Characterization of Rny1, the Saccharomyces cerevisiae member of the T-2 RNase family of RNases: unexpected functions for ancient enzymes? Proc Natl Acad Sci USA 98(3):1018–1023CrossRefPubMedGoogle Scholar
  49. McClure BA, Haring V et al (1989) Style self-incompatibility gene products of Nicotiana alata are ribonucleases. Nature 342(6252):955–957. doi:10.1038/342955a0 CrossRefPubMedGoogle Scholar
  50. Merchant SS, Prochnik SE et al (2007) The Chlamydomonas genome reveals the evolution of key animal and plant functions. Science 318(5848):245–250. doi:10.1126/science.1143609 CrossRefPubMedGoogle Scholar
  51. Nakai K, Horton P (1999) PSORT: a program for detecting sorting signals in proteins and predicting their subcellular localization. Trends Biochem Sci 24(1):34–35CrossRefPubMedGoogle Scholar
  52. Nasrallah JB (2005) Recognition and rejection of self in plant self-incompatibility: comparisons to animal histocompatibility. Trends Immunol 26(8):412–418CrossRefPubMedGoogle Scholar
  53. Nobuta K, Venu RC et al (2007) An expression atlas of rice mRNAs and small RNAs. Nat Biotechnol 25(4):473–477. doi:10.1038/Nbt1291 CrossRefPubMedGoogle Scholar
  54. O’hUigin C, Satta Y et al (2002) Contribution of homoplasy and of ancestral polymorphism to the evolution of genes in anthropoid primates. Mol Biol Evol 19(9):1501–1513PubMedGoogle Scholar
  55. Ohgi K, Iwama M et al (1996) Enzymatic activities of several K108 mutants of ribonuclease (RNase) isolated from Rhizopus niveus. Biol Pharm Bull 19(8):1080–1082PubMedGoogle Scholar
  56. Ohno H, Ehara Y (2005) Expression of ribonuclease gene in mechanically injured of virus-inoculated Nicotiana tabacum leaves. Tohoku J Agric Res 55(3–4):11Google Scholar
  57. Ouyang S, Zhu W et al (2007) The TIGR rice genome annotation resource: improvements and new features. Nucleic Acids Res 35:D883–D887. doi:10.1093/nar/gkl976 CrossRefPubMedGoogle Scholar
  58. Paterson AH, Bowers JE, et al (2009) The Sorghum bicolor genome and the diversification of grasses. Nature 457(7229):551–556. http://www.nature.com/nature/journal/v457/n7229/suppinfo/nature07723_S1.html Google Scholar
  59. Rensing SA, Lang D et al (2008) The Physcomitrella genome reveals evolutionary insights into the conquest of land by plants. Science 319(5859):64–69. doi:10.1126/science.1150646 CrossRefPubMedGoogle Scholar
  60. Rice Annotation Project (2008) The rice annotation project database (RAP-DB): 2008 update. Nucl Acids Res 36(Suppl 1):D1028–D1033. doi:10.1093/nar/gkm978
  61. Roalson EH, McCubbin AG (2003) S-RNases and sexual incompatibility: structure, functions, and evolutionary perspectives. Mol Phylogenet Evol 29(3):490–506. doi:10.1016/S1055-7903(03)00195-7 CrossRefPubMedGoogle Scholar
  62. Rogers SW, Rogers JC (1999) Cloning and characterization of a gibberellin-induced RNase expressed in barley aleurone cells. Plant Physiol 119(4):1457–1464CrossRefPubMedGoogle Scholar
  63. Rokas A, Carroll SB (2008) Frequent and widespread parallel evolution of protein sequences. Mol Biol Evol 25(9):1943–1953. doi:10.1093/molbev/msn143 CrossRefPubMedGoogle Scholar
  64. Rosenberg HF (1995) Recombinant human eosinophil cationic protein—ribonuclease-activity is not essential for cytotoxicity. J Biol Chem 270(14):7876–7881PubMedGoogle Scholar
  65. Salekdeh GH, Siopongco J et al (2002) Proteomic analysis of rice leaves during drought stress and recovery. Proteomics 2(9):1131–1145CrossRefPubMedGoogle Scholar
  66. Salse J, Bolot S et al (2008) Identification and characterization of shared duplications between rice and wheat provide new insight into grass genome evolution. Plant Cell 20(1):11–24. doi:10.1105/tpc.107.056309 CrossRefPubMedGoogle Scholar
  67. Sato K, Egami F (1957) Studies on ribonucleases in Takadiastase 1. J Biochem Tokyo 44(11):753–767Google Scholar
  68. Shoemaker RC, Schlueter J et al (2006) Paleopolyploidy and gene duplication in soybean and other legumes. Curr Opin Plant Biol 9(2):104–109. doi:10.1016/j.pbi.2006.01.007 CrossRefPubMedGoogle Scholar
  69. Smirnoff P, Roiz L et al (2006) A recombinant human RNASET2 glycoprotein with antitumorigenic and antiangiogenic characteristics: expression, purification, and characterization. Cancer 107(12):2760–2769. doi:10.1002/Cncr.22327 CrossRefPubMedGoogle Scholar
  70. Steinbachs JE, Holsinger KE (2002) S-RNase-mediated gametophytic self-incompatibility is ancestral in eudicots. Mol Biol Evol 19(6):825–829PubMedGoogle Scholar
  71. Swarbreck D, Wilks C, et al (2008) The Arabidopsis information resource (TAIR): gene structure and function annotation. Nucl Acids Res 36(Suppl 1): D1009–D1014. doi:10.1093/nar/gkm965
  72. Swofford DL (2002) PAUP*. Phylogenetic analysis using parsimony (*and other methods). Version 4.0b10. Sinauer Associates, SunderlandGoogle Scholar
  73. Tanaka N, Arai J et al (2000) Crystal structure of a plant ribonuclease, RNase LE. J Mol Biol 298(5):859–873. doi:10.1006/jmbi.2000.3707 CrossRefPubMedGoogle Scholar
  74. Taylor CB, Green PJ (1991) Genes with homology to fungal and S-Gene RNases are expressed in Arabidopsis thaliana. Plant Physiol 96(3):980–984. doi:10.1104/pp.96.3.980 CrossRefPubMedGoogle Scholar
  75. Taylor CB, Bariola PA et al (1993) Rns2—a senescence-associated Rnase of Arabidopsis that diverged from the S-Rnases before speciation. Proc Natl Acad Sci USA 90(11):5118–5122CrossRefPubMedGoogle Scholar
  76. Thompson DM, Parker R (2009) The RNase Rny1p cleaves tRNAs and promotes cell death during oxidative stress in Saccharomyces cerevisiae. J Cell Biol 185(1):43–50. doi:10.1083/jcb.200811119 CrossRefPubMedGoogle Scholar
  77. Torrent M, de la Torre BG et al (2009) Bactericidal and membrane disruption activities of the eosinophil cationic protein are largely retained in an N-terminal fragment. Biochem Jl 421(3):425–434. doi:10.1042/bj20082330 CrossRefGoogle Scholar
  78. Tuskan GA, DiFazio S, et al (2006) The genome of black cottonwood, Populus trichocarpa (Torr. & Gray). Science 313(5793):1596–1604. doi:10.1126/science.1128691
  79. Van Damme EJM, Hao Q et al (2000) Major protein of resting rhizomes of Calystegia sepium (hedge bindweed) closely resembles plant RNases but has no enzymatic activity. Plant Physiol 122(2):433–445CrossRefPubMedGoogle Scholar
  80. Verslues PE, Zhu J-K (2007) New developments in abscisic acid perception and metabolism. Curr Opin Plant Biol 10(5):447–452CrossRefPubMedGoogle Scholar
  81. Vieira J, Fonseca NA et al (2008) An S-RNase-based gametophytic self-incompatibility system evolved only once in eudicots. J Mol Evol 67(2):179–190. doi:10.1007/s00239-008-9137-x CrossRefPubMedGoogle Scholar
  82. Wei JY, Li AM et al (2006) Cloning and characterization of an RNase-related protein gene preferentially expressed in rice stems. Biosci Biotech Biochem 70(4):1041–1045CrossRefGoogle Scholar
  83. Whelan S, Goldman N (2001) A general empirical model of protein evolution derived from multiple protein families using a maximum-likelihood approach. Mol Biol Evol 18(5):691–699PubMedGoogle Scholar
  84. Yamane H, Tao R et al (2003) Identification of a non-S RNase, a possible ancestral form of S-RNases, in Prunus. Mol Genet Genomics 269(1):90–100. doi:10.1007/s00438-003-0815-5 PubMedGoogle Scholar
  85. Ye ZH, Droste DL (1996) Isolation and characterization of cDNAs encoding xylogenesis-associated and wounding-induced ribonucleases in Zinnia elegans. Plant Mol Biol 30(4):697–709CrossRefPubMedGoogle Scholar
  86. Zhang JZ (2003) Evolution by gene duplication: an update. Trends Ecol Evol 18(6):292–298. doi:10.1016/S0169-5347(03)00033-8 CrossRefGoogle Scholar
  87. Zhang JZ, Dyer KD et al (2000) Evolution of the rodent eosinophil-associated RNase gene family by rapid gene sorting and positive selection. Proc Natl Acad Sci USA 97(9):4701–4706CrossRefPubMedGoogle Scholar
  88. Zhang J, Dyer KD et al (2003) Human RNase 7: a new cationic ribonuclease of the RNase A superfamily. Nucleic Acids Res 31(2):602–607CrossRefPubMedGoogle Scholar
  89. Zimmermann P, Hennig L et al (2005) Gene-expression analysis and network discovery using Genevestigator. Trends Plant Sci 10(9):407–409CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag 2010

Authors and Affiliations

  • Gustavo C. MacIntosh
    • 1
    • 2
    • 3
  • Melissa S. Hillwig
    • 1
    • 2
  • Alexander Meyer
    • 1
    • 2
  • Lex Flagel
    • 4
  1. 1.Interdepartmental Genetics ProgramIowa State UniversityAmesUSA
  2. 2.Department of Biochemistry, Biophysics and Molecular BiologyIowa State UniversityAmesUSA
  3. 3.Plant Sciences InstituteIowa State UniversityAmesUSA
  4. 4.Department of Ecology, Evolution, and Organismal BiologyIowa State UniversityAmesUSA

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