Function and evolution of a microRNA that regulates a caspi2+-ATPase and triggers the formation of phased small interfering rnas in tomato reproductive Growth

Plant Cell

Volumn 23, Issue 9, 2011, Pages 3185-3203

  Wang, Ying ^a   Itaya, Asuka ^a,e   Zhong, Xuehua ^a,f   Wu, Yang ^b   Zhang, Jianfeng ^a,g   van der Knaap, Esther ^c   Olmstead, Richard ^d   Qi, Yijun ^b   Dinga, Biao ^a  

^a OHIO STATE UNIVERSITY   (United States)

^b NATIONAL INSTITUTE OF BIOLOGICAL SCIENCES   (China)

^c OHIO STATE UNIVERSITY   (United States)

^d UNIVERSITY OF WASHINGTON   (United States)

^e AGRICULTURE AND AGRI FOOD CANADA   (Canada)

^f UNIVERSITY OF CALIFORNIA   (United States)

^g UNIVERSITY OF TORONTO   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

EUKARYOTA; LYCOPERSICON ESCULENTUM; SOLANACEAE;

EID: 80055000264     PISSN: 10404651     EISSN: 1532298X     Source Type: Journal    
DOI: 10.1105/tpc.111.088013     Document Type: Article

References (95)

1. Ahn, D.H., Singaravelu, G., Lee, S., Ahnn, J., and Shim, Y.H. (2006). Functional and phenotypic relevance of differentially expressed proteins in calcineurin mutants of Caenorhabditis elegans. Proteomics 6: 1340-1350.
2. Allen, E., Xie, Z., Gustafson, A.M., and Carrington, J.C. (2005). MicroRNA-directed phasing during trans-acting siRNA biogenesis in plants. Cell 121: 207-221.
3. Allen, E., Xie, Z., Gustafson, A.M., Sung, G.H., Spatafora, J.W., and Carrington, J.C. (2004). Evolution of microRNA genes by inverted duplication of target gene sequences in Arabidopsis thaliana. Nat. Genet. 36: 1282-1290.
4. Axtell, M.J. (2008). Evolution of microRNAs and their targets: are all microRNAs biologically relevant? Biochim. Biophys. Acta 1779: 725-734.
5. Axtell, M.J., and Bowman, J.L. (2008). Evolution of plant microRNAs and their targets. Trends Plant Sci. 13: 343-349.
6. Axtell, M.J., Snyder, J.A., and Bartel, D.P. (2007). Common functions for diverse small RNAs of land plants. Plant Cell 19: 1750-1769.
7. Barakat, A., Wall, K., Leebens-Mack, J., Wang, Y.J., Carlson, J.E., and Depamphilis, C.W. (2007). Large-scale identification of micro- RNAs from a basal eudicot (Eschscholzia californica) and conservation in flowering plants. Plant J. 51: 991-1003.
8. 2+-ATPase. Phytochemistry 38: 15-17.
9. Baxter, I., Tchieu, J., Sussman, M.R., Boutry, M., Palmgren, M.G., Gribskov, M., Harper, J.F., and Axelsen, K.B. (2003). Genomic comparison of P-type ATPase ion pumps in Arabidopsis and rice. Plant Physiol. 132: 618-628.
10. Berger, Y., Harpaz-Saad, S., Brand, A., Melnik, H., Sirding, N., Alvarez, J.P., Zinder, M., Samach, A., Eshed, Y., and Ori, N. (2009). The NAC-domain transcription factor GOBLET specifies leaflet boundaries in compound tomato leaves. Development 136: 823-832.
11. Bologna, N.G., Mateos, J.L., Bresso, E.G., and Palatnik, J.F. (2009). A loop-to-base processing mechanism underlies the biogenesis of plant microRNAs miR319 and miR159. EMBO J. 28: 3646-3656.
12. Bonza, M.C., Morandini, P., Luoni, L., Geisler, M., Palmgren, M.G., and De Michelis, M.I. (2000). At-ACA8 encodes a plasma membranelocalized calcium-ATPase of Arabidopsis with a calmodulin-binding domain at the N terminus. Plant Physiol. 123: 1495-1506.
13. 2+pumps in plants. J. Bioenerg. Biomembr. 39: 409-414.
14. Buxdorf, K., Hendelman, A., Stav, R., Lapidot, M., Ori, N., and Arazi, T. (2010). Identification and characterization of a novel miR159 target not related to MYB in tomato. Planta 232: 1009-1022.
15. Carafoli, E. (2002). Calcium signaling: a tale for all seasons. Proc. Natl. Acad. Sci. USA 99: 1115-1122.
16. Carthew, R.W., and Sontheimer, E.J. (2009). Origins and mechanisms of miRNAs and siRNAs. Cell 136: 642-655.
17. 2+-ATPase in Arabidopsis thaliana seedlings. Plant Biol. (Stuttg.) 8: 572-578.
18. Chase, M.W., and Reveal, J.L. (2009). A phylogenetic classification of the land plants to accompany APG III. Bot. J. Linn. Soc. 161: 122-127.
19. Chen, H.M., Chen, L.T., Patel, K., Li, Y.H., Baulcombe, D.C., and Wu, S.H. (2010). 22-Nucleotide RNAs trigger secondary siRNA biogenesis in plants. Proc. Natl. Acad. Sci. USA 107: 15269-15274.
20. Chen, K.-Y., Cong, B., Wing, R., Vrebalov, J., and Tanksley, S.D. (2007). Changes in regulation of a transcription factor lead to autogamy in cultivated tomatoes. Science 318: 643-645.
21. Chen, X. (2009). Small RNAs and their roles in plant development. Annu. Rev. Cell Dev. Biol. 25: 21-44.
22. 2+)-ATPase (SCA1) that is located in the plasma membrane. Plant Cell 12: 1393-1407.
23. 2+ ATPases. J. Cell Biol. 124: 351-363.
24. Cuperus, J.T., Carbonell, A., Fahlgren, N., Garcia-Ruiz, H., Burke, R.T., Takeda, A., Sullivan, C.M., Gilbert, S.D., Montgomery, T.A., and Carrington, J.C. (2010). Unique functionality of 22-nt miRNAs in triggering RDR6-dependent siRNA biogenesis from target transcripts in Arabidopsis. Nat. Struct. Mol. Biol. 17: 997-1003.
25. Cuperus, J.T., Fahlgren, N., and Carrington, J.C. (2011). Evolution and functional diversification of MIRNA genes. Plant Cell 23: 431-442.
26. 2+ sensors in plant signalling. Biochem. J. 425: 27-40.
27. Dodd, A.N., Kudla, J., and Sanders, D. (2010). The language of calcium signaling. Annu. Rev. Plant Biol. 61: 593-620.
28. Fahlgren, N., Howell, M.D., Kasschau, K.D., Chapman, E.J., Sullivan, C.M., Cumbie, J.S., Givan, S.A., Law, T.F., Grant, S.R., Dangl, J.L., and Carrington, J.C. (2007). High-throughput sequencing of Arabidopsis microRNAs: Evidence for frequent birth and death of MIRNA genes. PLoS ONE 2: e219.
29. Fahlgren, N., Jogdeo, S., Kasschau, K.D., Sullivan, C.M., Chapman, E.J., Laubinger, S., Smith, L.M., Dasenko, M., Givan, S.A., Weigel, D., and Carrington, J.C. (2010). MicroRNA gene evolution in Arabidopsis lyrata and Arabidopsis thaliana. Plant Cell 22: 1074-1089.
30. Felippes, F.F., Schneeberger, K., Dezulian, T., Huson, D.H., and Weigel, D. (2008). Evolution of Arabidopsis thaliana microRNAs from random sequences. RNA 14: 2455-2459.
31. Floyd, S.K., and Bowman, J.L. (2004). Gene regulation: Ancient micro-RNA target sequences in plants. Nature 428: 485-486.
32. Geisler, M., Axelsen, K.B., Harper, J.F., and Palmgren, M.G. (2000). Molecular aspects of higher plant P-type Ca(2+)-ATPases. Biochim. Biophys. Acta 1465: 52-78.
33. 2+-ATPase regulates adult vegetative development and inflorescence architecture in Arabidopsis. Plant Physiol. 146: 716-728.
34. Hardingham, G.E., and Bading, H. (2003). The Yin and Yang of NMDA receptor signalling. Trends Neurosci. 26: 81-89.
35. Hepler, P.K. (2005). Calcium: A central regulator of plant growth and development. Plant Cell 17: 2142-2155.
36. Itaya, A., Bundschuh, R., Archual, A.J., Joung, J.G., Fei, Z., Dai, X., Zhao, P.X., Tang, Y., Nelson, R.S., and Ding, B. (2008). Small RNAs in tomato fruit and leaf development. Biochim. Biophys. Acta 1779: 99-107.
37. Johnson, C., Kasprzewska, A., Tennessen, K., Fernandes, J., Nan, G.L., Walbot, V., Sundaresan, V., Vance, V., and Bowman, L.H. (2009). Clusters and superclusters of phased small RNAs in the developing inflorescence of rice. Genome Res. 19: 1429-1440.
38. Joshi, T., Yan, Z., Libault, M., Jeong, D.H., Park, S., Green, P.J., Sherrier, D.J., Farmer, A., May, G., Meyers, B.C., Xu, D., and Stacey, G. (2010). Prediction of novel miRNAs and associated target genes in Glycine max. BMC Bioinformatics 11(Suppl. 1): S14.
39. Karimi, M., Inzé, D., and Depicker, A. (2002). GATEWAY vectors for Agrobacterium-mediated plant transformation. Trends Plant Sci. 7: 193-195.
40. Kasschau, K.D., Xie, Z.X., Allen, E., Llave, C., Chapman, E.J., Krizan, K.A., and Carrington, J.C. (2003). P1/HC-Pro, a viral suppressor of RNA silencing, interferes with Arabidopsis development and miRNA unction. Dev. Cell 4: 205-217.
41. Kim, V.N., Han, J., and Siomi, M.C. (2009). Biogenesis of small RNAs in animals. Nat. Rev. Mol. Cell Biol. 10: 126-139.
42. Kudla, J., Batistic, O., and Hashimoto, K. (2010). Calcium signals: The lead currency of plant information processing. Plant Cell 22: 541-563.
43. Kurihara, Y., Takashi, Y., and Watanabe, Y. (2006). The interaction between DCL1 and HYL1 is important for efficient and precise processing of pri-miRNA in plant microRNA biogenesis. RNA 12: 206-212.
44. Kurihara, Y., and Watanabe, Y. (2004). Arabidopsis micro-RNA biogenesis through Dicer-like 1 protein functions. Proc. Natl. Acad. Sci. USA 101: 12753-12758.
45. Kutter, C., Schö b, H., Stadler, M., Meins, F., Jr., and Si-Ammour, A. (2007). MicroRNA-mediated regulation of stomatal development in Arabidopsis. Plant Cell 19: 2417-2429.
46. Lelandais-Brière, C., Naya, L., Sallet, E., Calenge, F., Frugier, F., Hartmann, C., Gouzy, J., and Crespi, M. (2009). Genome-wide Medicago truncatula small RNA analysis revealed novel microRNAs and isoforms differentially regulated in roots and nodules. Plant Cell 21: 2780-2796.
47. Li, D., Wang, L., Wang, M., Xu, Y.Y., Luo, W., Liu, Y.J., Xu, Z.H., Li, J., and Chong, K. (2009). Engineering OsBAK1 gene as a molecular tool to improve rice architecture for high yield. Plant Biotechnol. J. 7: 791-806.
48. 2+-ATPase in Arabidopsis thaliana. Proc. Natl. Acad. Sci. USA 94: 8579-8584.
49. Llave, C., Xie, Z., Kasschau, K.D., and Carrington, J.C. (2002). Cleavage of Scarecrow-like mRNA targets directed by a class of Arabidopsis miRNA. Science 297: 2053-2056.
50. Lu, C., et al. (2008). Genome-wide analysis for discovery of rice microRNAs reveals natural antisense microRNAs (nat-miRNAs). Proc. Natl. Acad. Sci. USA 105: 4951-4956.
51. Lu, C., Kulkarni, K., Souret, F.F., MuthuValliappan, R., Tej, S.S., Poethig, R.S., Henderson, I.R., Jacobsen, S.E., Wang, W., Green, P.J., and Meyers, B.C. (2006). MicroRNAs and other small RNAs enriched in the Arabidopsis RNA-dependent RNA polymerase-2 mutant. Genome Res. 16: 1276-1288.
52. Lu, S., Sun, Y.H., Shi, R., Clark, C., Li, L., and Chiang, V.L. (2005). Novel and mechanical stress-responsive MicroRNAs in Populus trichocarpa that are absent from Arabidopsis. Plant Cell 17: 2186-2203.
53. Luo, X.B., Zhang, H.J., Xiao, J.N., and Wang, Z.G. (2010). Regulation of human cardiac ion channel genes by microRNAs: Theoretical perspective and pathophysiological implications. Cell. Physiol. Biochem. 25: 571-586.
54. Ma, Z., Coruh, C., and Axtell, M.J. (2010). Arabidopsis lyrata small RNAs: Transient MIRNA and small interfering RNA loci within the Arabidopsis genus. Plant Cell 22: 1090-1103.
55. Mahalingam, G., and Meyers, B.C. (2009). Computational methods for comparative analysis of plant small RNAs. In Plant MicroRNAs, Methods in Molecular Biology, B.C.M.a.P.J. Green, ed (New York: Humana Press), pp. 163-181.
56. Mallory, A.C., Reinhart, B.J., Jones-Rhoades, M.W., Tang, G., Zamore, P.D., Barton, M.K., and Bartel, D.P. (2004). MicroRNA control of PHABULOSA in leaf development: Importance of pairing to the microRNA 59 region. EMBO J. 23: 3356-3364.
57. Mateos, J.L., Bologna, N.G., Chorostecki, U., and Palatnik, J.F. (2010). Identification of microRNA processing determinants by random mutagenesis of Arabidopsis MIR172a precursor. Curr. Biol. 20: 49-54.
58. McAinsh, M.R., and Pittman, J.K. (2009). Shaping the calcium signature. New Phytol. 181: 275-294.
59. Meyers, B.C., et al. (2008). Criteria for annotation of plant microRNAs. Plant Cell 20: 3186-3190.
60. Molnár, A., Schwach, F., Studholme, D.J., Thuenemann, E.C., and Baulcombe, D.C. (2007). MiRNAs control gene expression in the single-cell alga Chlamydomonas reinhardtii. Nature 447: 1126-1129.
61. Montgomery, T.A., Yoo, S.J., Fahlgren, N., Gilbert, S.D., Howell, M.D., Sullivan, C.M., Alexander, A., Nguyen, G., Allen, E., Ahn, J.H., and Carrington, J.C. (2008). AGO1-miR173 complex initiates phased siRNA formation in plants. Proc. Natl. Acad. Sci. USA 105: 20055-20062.
62. Morin, R.D., Aksay, G., Dolgosheina, E., Ebhardt, H.A., Magrini, V., Mardis, E.R., Sahinalp, S.C., and Unrau, P.J. (2008). Comparative analysis of the small RNA transcriptomes of Pinus contorta and Oryza sativa. Genome Res. 18: 571-584.
63. Moxon, S., Jing, R., Szittya, G., Schwach, F., Rusholme Pilcher, R.L., Moulton, V., and Dalmay, T. (2008). Deep sequencing of tomato short RNAs identifies microRNAs targeting genes involved in fruit ripening. Genome Res. 18: 1602-1609.
64. 2+-ATPase is expressed differentially in phosphate-starved roots of tomato. Physiol. Plant. 101: 540-544.
65. Okada, C., Yamashita, E., Lee, S.J., Shibata, S., Katahira, J., Nakagawa, A., Yoneda, Y., and Tsukihara, T. (2009). A highresolution structure of the pre-microRNA nuclear export machinery. Science 326: 1275-1279.
66. Olmstead, R., Bohs, L., Migid, H., Santiago-Valentin, E., Garcia, V., and Collier, S. (2008). A molecular phylogeny of the Solanaceae. Taxon 57: 1159-1181.
67. Olmstead, R.G., Kim, K.J., Jansen, R.K., and Wagstaff, S.J. (2000). The phylogeny of the Asteridae sensu lato based on chloroplast ndhF gene sequences. Mol. Phylogenet. Evol. 16: 96-112.
68. Ori, N., et al. (2007). Regulation of LANCEOLATE by miR319 is required for compound-leaf development in tomato. Nat. Genet. 39: 787-791.
69. Park, W., Li, J., Song, R., Messing, J., and Chen, X. (2002). CARPEL FACTORY, a Dicer homolog, and HEN1, a novel protein, act in microRNA metabolism in Arabidopsis thaliana. Curr. Biol. 12: 1484-1495.
70. Pilcher, R.L.R., Moxon, S., Pakseresht, N., Moulton, V., Manning, K., Seymour, G., and Dalmay, T. (2007). Identification of novel small RNAs in tomato (Solanum lycopersicum). Planta 226: 709-717.
71. Rajagopalan, R., Vaucheret, H., Trejo, J., and Bartel, D.P. (2006). A diverse and evolutionarily fluid set of microRNAs in Arabidopsis thaliana. Genes Dev. 20: 3407-3425.
72. Reinhart, B.J., Weinstein, E.G., Rhoades, M.W., Bartel, B., and Bartel, D.P. (2002). MicroRNAs in plants. Genes Dev. 16: 1616-1626.
73. 2+-ATPase are a dimer and a monomercalmodulin complex. J. Biol. Chem. 271: 9987-9991.
74. Salomonis, N., et al. (2010). Alternative splicing regulates mouse embryonic stem cell pluripotency and differentiation. Proc. Natl. Acad. Sci. USA 107: 10514-10519.
75. Sanders, D., Brownlee, C., and Harper, J.F. (1999). Communicating with calcium. Plant Cell 11: 691-706.
76. Sanders, D., Pelloux, J., Brownlee, C., and Harper, J.F. (2002). Calcium at the crossroads of signaling. Plant Cell 14(Suppl): S401-S417.
77. 2+pumps expressed in stomatal guard cells show opposite expression patterns during cold stress. Physiol. Plant. 124: 278-283.
78. 2+ pump is required for normal pollen tube growth and fertilization. Proc. Natl. Acad. Sci. USA 101: 9502-9507.
79. Schwab, R., Ossowski, S., Riester, M., Warthmann, N., and Weigel, D. (2006). Highly specific gene silencing by artificial microRNAs in Arabidopsis. Plant Cell 18: 1121-1133.
80. Song, L., Axtell, M.J., and Fedoroff, N.V. (2010). RNA secondary structural determinants of miRNA precursor processing in Arabidopsis. Curr. Biol. 20: 37-41.
81. Sunkar, R., and Jagadeeswaran, G. (2008). In silico identification of conserved microRNAs in large number of diverse plant species. BMC Plant Biol. 8: 37.
82. 2+ pumps: Insights from expression in yeast. Annu. Rev. Plant Physiol. Plant Mol. Biol. 51: 433-462.
83. Szittya, G., Moxon, S., Santos, D.M., Jing, R., Fevereiro, M.P., Moulton, V., and Dalmay, T. (2008). High-throughput sequencing of Medicago truncatula short RNAs identifies eight new miRNA families. BMC Genomics 9: 593.
84. 2+ transport in the sarcoplasmic reticulum. Biochem. J. 414: 357-361.
85. Voinnet, O. (2009). Origin, biogenesis, an d activity of plant microRNAs. Cell 136: 669-687.
86. Wang, L., Xu, Y.Y., Li, J., Powell, R.A., Xu, Z.H., and Chong, K. (2007a). Transgenic rice plants ectopically expressing AtBAK1 are semi-dwarfed and hypersensitive to 24-epibrassinolide. J. Plant Physiol. 164: 655-664.
87. Wang, Y., Zhong, X., Itaya, A., and Ding, B. (2007b). Evidence for the existence of the loop E motif of Potato spindle tuber viroid in vivo. J. Virol. 81: 2074-2077.
88. Wei, B., Cai, T., Zhang, R., Li, A., Huo, N., Li, S., Gu, Y.Q., Vogel, J., Jia, J., Qi, Y., and Mao, L. (2009). Novel microRNAs uncovered by deep sequencing of small RNA transcriptomes in bread wheat (Triticum aestivum L.) and Brachypodium distachyon (L.) Beauv. Funct. Integr. Genomics 9: 499-511.
89. Werner, S., Wollmann, H., Schneeberger, K., and Weigel, D. (2010). Structure determinants for accurate processing of miR172a in Arabidopsis thaliana. Curr. Biol. 20: 42-48.
90. Wimmers, L.E., Ewing, N.N., and Bennett, A.B. (1992). Higher plant Ca(2+)-ATPase: Primary structure and regulation of mRNA abundance by salt. Proc. Natl. Acad. Sci. USA 89: 9205-9209.
91. Yoshikawa, M., Peragine, A., Park, M.Y., and Poethig, R.S. (2005). A pathway for the biogenesis of trans-acting siRNAs in Arabidopsis. Genes Dev. 19: 2164-2175.
92. Zhang, B., Wang, Q., and Pan, X. (2007). MicroRNAs and their regulatory roles in animals and plants. J. Cell. Physiol. 210: 279-289.
93. Zhao, T., Li, G., Mi, S., Li, S., Hannon, G.J., Wang, X.J., and Qi, Y. (2007). A complex system of small RNAs in the unicellular green alga Chlamydomonas reinhardtii. Genes Dev. 21: 1190-1203.
94. Zhu, Q.H., Spriggs, A., Matthew, L., Fan, L., Kennedy, G., Gubler, F., and Helliwell, C. (2008). A diverse set of microRNAs and microRNAlike small RNAs in developing rice grains. Genome Res. 18: 1456-1465.
95. Zuker, M. (2003). Mfold web server for nucleic acid folding and hybridization prediction. Nucleic Acids Res. 31: 3406-3415.