Expression and tissue-specific localization of nitrate-responsive miRNAs in roots of maize seedlings

Plant, Cell and Environment

Volumn 35, Issue 6, 2012, Pages 1137-1155

  Trevisan, Sara ^a   Nonis, Alberto ^a   Begheldo, Maura ^a   Manoli, Alessandro ^a   Palme, Klaus ^b   Caporale, Giovanni ^a   Ruperti, Benedetto ^a   Quaggiotti, Silvia ^a  

^a UNIVERSITY OF PADOVA   (Italy)

^b UNIVERSITY OF FREIBURG   (Germany)

Author keywords

MiRNAs; Nitrate signalling; Roots; Spatio temporal expression; Zea mays L

Indexed keywords

MICRORNA; NITRATE; PLANT RNA;

ADAPTATION; CROP PRODUCTION; ECOMORPHOLOGY; MAIZE; METABOLISM; MOLECULAR ANALYSIS; NITRATE; NITROGEN; NUTRIENT USE EFFICIENCY; OPTIMIZATION; PHYSIOLOGICAL RESPONSE; POLYMERASE CHAIN REACTION; REAL TIME; ROOT; SEEDLING; SURVIVAL;

ARTICLE; DNA PROBE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETICS; IN SITU HYBRIDIZATION; MAIZE; METABOLISM; PLANT ROOT; PROMOTER REGION; REAL TIME POLYMERASE CHAIN REACTION;

DNA PROBES; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, PLANT; IN SITU HYBRIDIZATION; MICRORNAS; NITRATES; PLANT ROOTS; PROMOTER REGIONS, GENETIC; REAL-TIME POLYMERASE CHAIN REACTION; RNA, PLANT; ZEA MAYS;

ZEA MAYS;

EID: 84860257793     PISSN: 01407791     EISSN: 13653040     Source Type: Journal    
DOI: 10.1111/j.1365-3040.2011.02478.x     Document Type: Article

References (89)

1. Abdel-Ghany S.E. & Pilon M. (2008) MicoRNA-mediated systemic down-regulation of copper protein expression in response to low copper availability in Arabidopsis. The Journal of Biological Chemistry 283, 15932-15945.
2. Ahuja I., de Vos R.C., Bones A.M. & Hall R.D. (2010) Plant molecular stress responses face climate change. Trends in Plant Science 15, 664-674.
3. Bari R., Datt Pant B., Stitt M. & Scheible W.R. (2006) PHO2, microRNA399, and PHR1 define a phosphate-signaling pathway in plants. Plant Physiology 141, 988-999.
4. Boualem A., Laporte P., Jovanovic M., Laffont C., Plet J., Combier J.P., Niebel A., Crespi M. & Frugier F. (2008) MicroRNA166 controls root and nodule development in Medicago truncatula. The plant Journal 54, 876-878.
5. Burkhead J.L., Reynolds K.A., Abdel-Ghany S.E., Cohu C.M. & Pilon M. (2009) Copper homeostasis. The New Phytologist 182, 799-816.
6. Camargo J.A. & Alonso A. (2006) Ecological and toxicological effects of inorganic nitrogen pollution in aquatic ecosystems: a global assessment. Environment International 32, 831-849.
7. Canãs L.A., Busscher M., Angenent G.C., Beltran J.P. & van Tunen A.J. (1994) Nuclear localization of the Petunia MADS box protein FBP1. The Plant Journal 6, 597-604.
8. Carlsbecker A., Lee J.Y., Roberts C.J., etal. (2010) Cell signalling by microRNA165/6 directs gene dose-dependent root cell fate. Nature 465, 316-321.
9. Chang W.C., Lee T.Y., Huang H.D., Huang H.Y. & Pan R.L. (2008) PlantPAN: plant promoter analysis navigator, for identifying combinatorial cis-regulatory elements with distance constraint in plant gene groups. BMC Genomics 9, 561.
10. Chiou T.J. (2007) The role of microRNAs in sensing nutrient stress. Plant, Cell and Environment 30, 323-332.
11. Combier J.P., Frugier F., de Billy F., etal. (2006) MtHAP2-1 is a key transcriptional regulator of symbiotic nodule development regulated by microRNA169 in Medicago truncatula. Genes & Development 20, 3084-3088.
12. Dai X. & Zhao P.X. (2011) psRNATarget: a Plant small RNA target analysis server Nucleic Acids Research doi: 10.1093/nar/GKR319.
13. Darnell D.K., Stanislaw S., Kaur S. & Antin P.B. (2010) Whole mount in situ hybridization detection of mRNAs using short LNA containing DNA oligonucleotide probes. RNA 16, 632-637.
14. Dezulian T., Palatnik J.F., Huson D.H. & Weigel D. (2005) Conservation and divergence of microRNA families in plants. Genome Biology 6, 13.
15. Einsle O., Mehrabian Z., Nalbandyan R. & Messerschmidt A. (2000) Crystal structure of plantacyanin, a basic blue cupredoxin from spinach. Society of Biological Inorganic Chemistry 5, 666-672.
16. Emery J.F., Floyd S.K., Alvarez J., Eshed Y., Hawker N.P., Izhaki A., Baum S.F. & Bowman J.L. (2003) Radial patterning of Arabidopsis shoots by class III HD-ZIP and KANADI genes. Current Biology 13, 1768-1774.
17. Friml J., Vieten A., Sauer M., Weijers D., Schwarz H., Hamann T., Offringa R. & Jürgens G. (2003) Efflux-dependent auxin gradients establish the apical-basal axis of Arabidopsis. Nature 426, 147-153.
18. Fujii H., Chiou T.J., Lin S.I., Aung K. & Zhu J.K. (2005) A miRNA involved in phosphate-starvation response in Arabidopsis. Current Biology 15, 2038-2043.
19. Galloway J.N., Aber J.D., Erisman J.W., Seitzinger S.P., Howarth R.H., Cowling E.B. & Cosby B.J. (2003) The nitrogen cascade. Bioscience 53, 341-356.
20. Gardiner J., Sherr I. & Scarpella E. (2010) Expression of DOF genes identifies early stages of vascular development in Arabidopsis leaves. The International Journal of Developmental Biology 54, 1389-1396.
21. German M.A., Pillay M., Jeong D.H., etal. (2008) Global identification of microRNA-target RNA pairs by parallel analysis of RNA ends. Nature Biotechnology 26, 941-946.
22. Gifford M.L., Dean A., Gutierrez R.A., Coruzzi G.M. & Birnbaum K.D. (2008) Cell-specific nitrogen responses mediate developmental plasticity. Proceedings of the National Academy of Sciences of the United States of America 105, 803-808.
23. Good A.G., Shrawat A.K. & Muench D.G. (2004) Can less yield more? Is reducing nutrient input into the environment compatible with maintaining crop production? Trends in Plant Science 9, 597-605.
24. Griffiths-Jones S., Saini H.K., van Dongen S. & Enright A.J. (2008) miRBase: tools for microRNA genomics. Nucleic Acids Research 36, D154-D158.
25. Guss J.M., Merritt E.A., Phizackerley R.P. & Freeman H.S. (1996) The structure of a phytocyanin, the basic blue protein from cucumber, refined at 1.8 A resolution. Journal of Molecular Biology 262, 686-670.
26. Gutiérrez R.A., Gifford M.L., Poultney C., Wang R., Shasha D.E., Coruzzi G.M. & Crawford N.M. (2007) Insights into the genomic nitrate response using genetics and the Sungear Software System. Journal of Experimental Botany 58, 2359-2367.
27. Hadfi K., Speth V. & Neuhaus G. (1998) Auxin-induced developmental patterns in Brassica juncea embryos. Development 125, 879-887.
28. Hirel B., Le Gouis J., Ney B. & Gallais A. (2007) The challenge of improving nitrogen use efficiency in crop plants: towards a more central role for genetic variability and quantitative genetics within integrated approaches. Journal of Experimental Botany 58, 2369-2387.
29. Ho C.H., Lin S.H., Hu H.C. & Tsay Y.F. (2009) CHL1 functions as a nitrate sensor in plants. Cell 138, 1184-1194.
30. Hsieh L.C., Lin S.I., Shih A.C., Chen J.W., Lin W.Y., Tseng C.Y., Li W.H. & Chiou T.J. (2009) Uncovering small RNA-mediated responses to phosphate deficiency in Arabidopsis by deep sequencing. Plant Physiology 151, 2120-2132.
31. Hunt P.W., Watts R.A., Trevaskis B., Llewelyn D.J., Burnell J., Dennis E.S. & Peacock W.J. (2001) Expression and evolution of functionally distinct haemoglobin genes in plants. Plant Molecular Biology 47, 677-679.
32. Hwang H.W., Wentzel E.A. & Mendell J.T. (2007) A hexanucleotide element directs microRNA nuclear import. Science 315, 97-100.
33. Jagadeeswaran G., Zheng Y., Sumathipala N., Jiang H., Arrese E.L., Soulages J.L., Zhang W. & Sunkar R. (2010) Deep sequencing of small RNA libraries reveals dynamic regulation of conserved and novel microRNAs and microRNA-stars during silkworm development. BMC Genomics 20, 11-52.
34. Johnston T. & Chiotti Q. (2000) Climate change and the adaptability of agriculture: a review. Journal of the Air & Waste Management Association 50, 563-569.
35. Jones-Rhoades M.W. & Bartel D.P. (2004) Computational identification of plant microRNAs and their targets, including a stress-induced miRNA. Molecular Cell 14, 787-799.
36. Juarez M.T., Kui J.S., Thomas J., Heller B.A. & Timmermans M.C. (2004) microRNA-mediated repression of rolled leaf1 specifies maize leaf polarity. Nature 428, 84-88.
37. Kawashima C.G., Yoshimoto N., Maruyama-Nakashita A., Tsuchiya Y.N., Saito K., Takahashi H. & Dalmay T. (2009) Sulphur starvation induces the expression of microRNA-395 and one of its target genes but in different cell types. The Plant Journal 2, 313-321.
38. Kidner C.A. & Martienssen R.A. (2005) The developmental role of microRNA in plants. Current Opinion in Plant Biology 8, 38-44.
39. Kim J., Jung J.H., Reyes J.L., etal. (2005) MicroRNA-directed cleavage of ATHB15 mRNA regulates vascular development in Arabidopsis inflorescence stems. The Plant Journal 42, 84-94.
40. Kloosterman W.P., Wienholds E., de Bruijn E., Kauppinen S. & Plasterk R.H.A (2006) In situ detection of miRNAs in animal embryos using LNA-modified oligonucleotide probes. Nature Methods 3, 27-29.
41. Lasswell J., Rogg L.E., Nelson D.C., Rongey C. & Bartel B. (2000) Cloning and characterization of IAR1, a gene required for auxin conjugate sensitivity in Arabidopsis. The Plant Cell 12, 2395-2408.
42. Li A., Wang X., Leseberg C.H., Jia J. & Mao L. (2008) Biotic and abiotic stress responses through calcium-dependent protein kinase (CDPK) signaling in wheat (Triticum aestivum L.). Plant Signaling and Behaviour 3, 654-656.
43. 2-responsive miRNAs and 32 new miRNAs in the seedlings of rice (Oryza sativa L. ssp. indica). Nucleic Acids Research 39, 2821-2833.
44. Li Y.F., Zheng Y., Addo-Quaye C., Zhang L., Saini A., Jagadeeswaran G., Axtell M.J., Zhang W. & Sunkar R. (2010) Transcriptome-wide identification of microRNA targets in rice. The Plant Journal 62, 742-759.
45. Lijavetzky D., Carbonero P. & Vicente-Carbajosa J. (2003) Genome-wide comparative phylogenetic analysis of the rice and Arabidopsis Dof gene families. BMC Evolutionary Biology 23, 3-17.
46. Liu C., Xu Z. & Chua N.H. (1993) Auxin polar transport is essential for the establishment of bilateral symmetry during early plant embryogenesis. The Plant Cell 5, 621-630.
47. Mantovani R. (1999) The molecular biology of the CCAAT-binding factor NF-Y. Gene 239, 15-27.
48. Masclaux-Daubresse C., Daniel-Vedele F., Dechorgnat J., Chardon F., Gaufichon L. & Suzuki A. (2010) Nitrogen uptake, assimilation and remobilization in plants: challenges for sustainable and productive agriculture. Annals of Botany 105, 1141-1157.
49. Mittler R. (2006) Abiotic stress, the field environment and stress combination. Trends in Plant Science 11, 15-19.
50. Mittler R. & Blumwald E. (2010) Genetic engineering for modern agriculture: challenges and perspectives. Annual Review of Plant Biology 61, 443-462.
51. Mockaitis K. & Estelle M. (2008) Auxin receptors and plant development: a new signaling paradigm. Annual Review of Cell and Developmental Biology 24, 55-80.
52. Nelson D.E., Repetti P.P., Adams T.R., etal. (2007) Plant nuclear factor Y (NF-Y) B subunits confer drought tolerance and lead to improved corn yields on water-limited acres. Proceedings of the National Academy of Sciences of the United States of America 104, 16450-16455.
53. Noir R., Kotera M., Pons B., Remy J.S. & Behr J.P. (2008) Oligonucleotide- Oligospermine conjugates (Zip Nucleic Acids): a convenient means of finely tuning hybridization temperatures. Journal of the American Chemical Society 130, 13500-13505.
54. Nolan T., Hands R.E. & Bustin S.A. (2006) Quantification of mRNA using real-time RT-PCR. Nature Protocols 1, 1559-1582.
55. Okamura K., Phillips M.D., Tyler D.M., Duan H., Chou Y.T. & Lai E.C. (2008) The regulatory activity of microRNA* species has substantial influence on microRNA and 3′ UTR evolution. Nature Structural & Molecular Biology 15, 354-363.
56. Packer A.N., Xing Y., Harper S.Q., Jones L. & Davidson B.L. (2008) The bifunctional microRNA miR-9/miR-9* regulates REST and CoREST and is downregulated in Huntington's disease. The Journal of Neuroscience 28, 14341-14346.
57. Palenchar P.M., Kouranov A., Lejay L.V. & Coruzzi G.M. (2004) Genome-wide patterns of carbon and nitrogen regulation of gene expression validate the combined carbon and nitrogen (CN)-signaling hypothesis in plants. Genome Biology 5, R91.
58. Pant B.D., Musialak-Lange M., Nuc P., May P., Buhtz A., Kehr J., Walther D. & Scheible W.R. (2009) Identification of nutrient-responsive Arabidopsis and rapeseed microRNAs by comprehensive real-time polymerase chain reaction profiling and small RNA sequencing. Plant Physiology 150, 1541-1555.
59. Peoples M.B., Herridge D.F. & Ladha J.K. (1995) Biological nitrogen fixation: an efficient source of nitrogen for sustainable agricultural production. Plant and Soil 174, 3-28.
60. Péret B., Larrieu A. & Bennett M.J. (2009) Lateral root emergence: a difficult birth. Journal of Experimental Botany 60, 3637-3643.
61. Politz J.C., Zhang F. & Pederson T. (2006) MicroRNA-206 colocalizes with ribosome-rich regions in both the nucleolus and cytoplasm of rat myogenic cells. Proceedings of the National Academy of Sciences of the United States of America 103, 18957-18962.
62. Politz J.C., Hogan E.M. & Pederson T. (2009) MicroRNAs with a nucleolar location. RNA 15, 1705-1715.
63. Prigge M.J., Otsuga D., Alonso J.M., Ecker J.R., Drews G.N. & Clark S.E. (2005) Class III homeodomain-leucine zipper gene family members have overlapping, antagonistic, and distinct roles in Arabidopsis development. The Plant Cell 17, 61-76.
64. +-ATPase in relation to whole plant nitrate transport physiology in two maize genotypes differently responsive to low nitrogen availability. Journal of Experimental Botany 54, 1023-1031.
65. Ross E.J., Stone J.M., Elowsky C.G., Arredondo-Peter R., Klucas R.V. & Sarath G. (2004) Activation of the Oryza sativa non-symbiotic haemoglobin-2 promoter by the cytokinin-regulated transcription factor, ARR1. Journal of Experimental Botany 55, 1721-1731.
66. Raymond C.K., Roberts B.S., Garrett-Engele P., Lim L.P. & Johnson J.M. (2005) Simple, quantitative primer-extension PCR assay for direct monitoring of microRNAs and short-interfering RNAs. RNA 11, 1737-1744.
67. Saccomani M., Stevanato P., Trebbi D., McGrath M. & Biancardi E. (2009) Molecular and morpho-physiological characterization of sea, ruderal and cultivated beets. Euphytica 169, 19-29.
68. Schachtman D.P. & Shin R. (2007) Nutrient sensing and signaling: NPKS. Annual Review of Plant Biology 58, 47-69.
69. Shi R. & Chiang V.L. (2005) Facile means for quantifying microRNA expression by real-time PCR. Biotechniques 39, 519-525.
70. Shin R., Berg R.H. & Schachtman D.P. (2005) Reactive oxygen species and root hairs in Arabidopsis root response to nitrogen, phosphorus and potassium deficiency. Plant and Cell Physiology 46, 1350-1357.
71. Shukla L.I., Chinnusamy V. & Sunkar R. (2008) The role of microRNAs and other endogenous small RNAs in plant stress responses. Biochimica et Biophysica Acta 1779, 743-748.
72. Smith T.F. & Waterman M.S. (1981) Identification of Common Molecular Subsequences. Journal of Molecular Biology 147, 195-197.
73. Sreenivasulu N., Sopory S.K. & Kavi Kishor P.B. (2007) Deciphering the regulatory mechanisms of abiotic stress tolerance in plants by genomic approaches. Gene 388, 1-13.
74. Sunkar R. (2010) MicroRNAs with macro-effects on plant stress responses. Seminars in Cell & Developmental Biology 21, 805-811.
75. Sunkar R., Chinnusamy V., Zhu J. & Zhu J.K. (2007) Small RNAs as big players in plant abiotic stress responses and nutrient deprivation. Trends in Plant Science 12, 301-309.
76. Trevisan S., Borsa P., Botton A., Varotto S., Malagoli M., Ruperti B. & Quaggiotti S. (2008) Expression of two maize putative nitrate transporters in response to nitrate and sugar availability. The Plant Biology 10, 462-475.
77. Trevisan S., Manoli A., Begheldo M., Nonis A., Enna M., Vaccaro S., Caporale G., Ruperti B. & Quaggiotti S. (2011) Transcriptome analysis reveals coordinated spatiotemporal regulation of hemoglobin and nitrate reductase in response to nitrate in maize roots. New Phytologist 192, 338-352.
78. Trindade I., Capitão C., Dalmay T., Fevereiro M.P. & Santos D.M. (2010) miR398 and miR408 are up-regulated in response to water deficit in Medicago truncatula. Planta 231, 705-716.
79. Válóczi A., Várallyay E., Kauppinen S., Burgyán J. & Havelda Z. (2006) Spatio- temporal accumulation of microRNAs is highly coordinated in developing plant tissues. The Plant Journal 47, 140-151.
80. Vidal E.A., Araus V., Lu C., Parry G., Green P.J., Coruzzi G.M. & Gutiérrez R.A. (2010) Nitrate-responsive miR393/AFB3 regulatory module controls root system architecture in Arabidopsis thaliana. Proceedings of the National Academy of Sciences of the United States of America 107, 4477-4482.
81. Wang R., Tischner R., Gutiérrez R.A., Hoffman M., Xing X., Chen M., Coruzzi G. & Crawford N.M. (2004) Genomic analysis of the nitrate response using a nitrate reductase-null mutant of Arabidopsis. Plant Physiology 136, 2512-2522.
82. Wang R., Xing X. & Crawford N. (2007) Nitrite acts as a transcriptome signal at micromolar concentrations in Arabidopsis roots. Plant Physiology 145, 1735-1745.
83. Wong C.E., Zhao Y.T., Wang X.J., Croft L., Wang Z.H., Haerizadeh F., Mattick J.S., Singh M.B., Carroll B.J. & Bhalla P.L. (2011) MicroRNAs in the shoot apical meristem of soybean. Journal of Experimental Botany 62, 2495-2506.
84. Yamasaki H., Abdel-Ghany S.E., Cohu C.M., Kobayashi Y., Shikanai T. & Pilon M. (2007) Regulation of copper homeostasis by micro-RNA in Arabidopsis. The Journal of Biological Chemistry 282, 16369-16378.
85. Yanagisawa S., Akiyama A., Kisaka H., Uchimiya H. & Miwa T. (2004) Metabolic engineering with Dof1 transcription factor in plants: improved nitrogen assimilation and growth under low-nitrogen conditions. Proceedings of the National Academy of Sciences of the United States of America 101, 7833-7838.
86. You Y., Moreira B.G., Behlke M.A. & Owczarzy R. (2006) Design of LNA probes that improve mismatch discrimination. Nucleic Acids Research 34, e60.
87. Zanetti M.E., Blanco F.A., Beker M.P., Battaglia M. & Aguilar O.M. (2010) A C subunit of the plant nuclear factor NF-Y required for rhizobial infection and nodule development affects partner selection in the common bean-Rhizobium etli symbiosis. The Plant Cell 22, 4142-4157.
88. Zhang L., Chia J.M., Kumari S. etal. (2009) A genome-wide characterization of microRNA genes in maize. PLoS Genetics 5, e1000716.
89. Zhao M., Ding H., Zhu J.K., Zhang F. & Li W.X. (2011) Involvement of miR169 in the nitrogen-starvation responses in Arabidopsis. New Phytologist 190, 906-915.