Hypoxia-responsive microRNAs and trans-acting small interfering RNAs in Arabidopsis

Journal of Experimental Botany

Volumn 61, Issue 1, 2010, Pages 165-177

  Moldovan, Dov ^a,b   Spriggs, Andrew ^a   Yang, Jun ^a   Pogson, Barry J ^b   Dennis, Elizabeth S ^a   Wilson, Iain W ^a  

^a CSIRO   (Australia)

^b AUSTRALIAN NATIONAL UNIVERSITY   (Australia)

Author keywords

Abiotic stress; Arabidopsis thaliana; Deep sequencing; Hypoxia; MicroRNA; Mitochondria; Trans acting small interfering RNA

Indexed keywords

MESSENGER RNA; MICRORNA; SMALL INTERFERING RNA;

ARABIDOPSIS; ARTICLE; BIOLOGICAL MODEL; CELL HYPOXIA; CELL RESPIRATION; CYTOLOGY; DNA SEQUENCE; GENE EXPRESSION REGULATION; GENETICS; HIGH THROUGHPUT SCREENING; METABOLISM; MITOCHONDRION; NUCLEOTIDE SEQUENCE; PHYSIOLOGICAL STRESS; PLANT ROOT; POLYMERASE CHAIN REACTION; PROMOTER REGION;

ARABIDOPSIS; BASE SEQUENCE; CELL HYPOXIA; CELL RESPIRATION; GENE EXPRESSION REGULATION, PLANT; HIGH-THROUGHPUT SCREENING ASSAYS; MICRORNAS; MITOCHONDRIA; MODELS, BIOLOGICAL; PLANT ROOTS; POLYMERASE CHAIN REACTION; PROMOTER REGIONS, GENETIC; RNA, MESSENGER; RNA, SMALL INTERFERING; SEQUENCE ANALYSIS, DNA; STRESS, PHYSIOLOGICAL;

ARABIDOPSIS; ARABIDOPSIS THALIANA;

EID: 72049103210     PISSN: 00220957     EISSN: 14602431     Source Type: Journal    
DOI: 10.1093/jxb/erp296     Document Type: Article

References (78)

1. 2 stress response in plants. Critical Reviews in Plant Sciences 25, 1-21.
2. Allen E, Xie ZX, Gustafson AM, Carrington JC. 2005. microRNA-directed phasing during trans-acting siRNA biogenesis in plants. Cell 121, 207-221.
3. Andres C, Lurin C, Small ID. 2007. The multifarious roles of PPR proteins in plant mitochondrial gene expression. Physiologia Plantarum 129, 14-22.
4. Aukerman MJ, Sakai H. 2003. Regulation of flowering time and floral organ identity by a microRNA and its APETALA2-like target genes. The Plant Cell 15, 2730-2741.
5. Bailey-Serres J, Chang R. 2005. Sensing and signalling in response to oxygen deprivation in plants and other organisms. Annals of Botany 96, 507-518.
6. Bailey-Serres J, Voesenek LACJ. 2008. Flooding stress: acclimations and genetic diversity. Annual Review of Plant Biology 59, 313-339.
7. Baxter-Burrell A, Yang ZB, Springer PS, Bailey-Serres J. 2002. RopGAP4-dependent Rop GTPase rheostat control of Arabidopsis oxygen deprivation tolerance. Science 296, 2026-2028.
8. Bazzini AA, Hopp HE, Beachy RN, Asurmendi S. 2007. Infection and co-accumulation of tobacco mosaic virus proteins alter microRNA levels, correlating with symptom and plant development. Proceedings of the National Academy of Sciences, USA 104, 12157-12162.
9. Bond DM, Wilson IW, Dennis ES, Pogson BJ, Finnegan EJ. 2009. VERNALIZATION INSENSITIVE 3 (VIN3) is required for the response of Arabidopsis thaliana seedlings exposed to low oxygen conditions. The Plant Journal 59, 576-587.
10. Bonnet E, Van de Peer Y, Rouz P. 2006. The small RNA world of plants. New Phytologist 171, 451-468.
11. Borsani O, Zhu J, Verslues PE, Sunkar R, Zhu JK. 2005. Endogenous siRNAs derived from a pair of natural cis-antisense transcripts regulate salt tolerance in Arabidopsis. Cell 123, 1279-1291.
12. Boualem A, Laporte P, Jovanovic M, Laffont C, Plet J, Combier JP, Niebel A, Crespi M, Frugier F. 2008. MicroRNA166 controls root and nodule development in Medicago truncatula. The Plant Journal 54, 876-887.
13. Boyer JS. 1982. Plant productivity and environment. Science 218, 443-448.
14. Branco-Price C, Kaiser KA, Jang CJH, Larive CK, Bailey-Serres J. 2008. Selective mRNA translation coordinates energetic and metabolic adjustments to cellular oxygen deprivation and reoxygenation in Arabidopsis thaliana. The Plant Journal 56, 743-755.
15. Branco-Price C, Kawaguchi R, Ferreira RB, Bailey-Serres J. 2005. Genome-wide analysis of transcript abundance and translation in arabidopsis seedlings subjected to oxygen deprivation. Annals of Botany 96, 647-660.
16. Brodersen P, Sakvarelidze-Achard L, Bruun-Rasmussen M, Dunoyer P, Yamamoto YY, Sieburth L, Voinnet O. 2008. Widespread translational inhibition by plant miRNAs and siRNAs. Science 320, 1185-1190.
17. Chang WC, Lee TY, Huang HD, Huang HY, Pan RL. 2008. PlantPAN: plant promoter analysis navigator, for identifying combinatorial cis-regulatory elements with distance constraint in plant gene groups. BMC Genomics 9, 561.
18. Chen C, Ridzon DA, Broomer AJ, et al. 2005. Real-time quantification of microRNAs by stem-loop RT-PCR. Nucleic Acids Research 33, e179.
19. Christianson JA, Wilson IW, Llewellyn DJ, Dennis ES. 2009. The low-oxygen-induced NAC domain transcription factor ANAC102 affects viability of Arabidopsis seeds following low-oxygen treatment. Plant Physiology 149, 1724-1738.
20. Czechowski T, Stitt M, Altmann T, Udvardi MK, Scheible WR. 2005. Genome-wide identification and testing of superior reference genes for transcript normalization in Arabidopsis. Plant Physiology 139, 5-17.
21. Ding D, Zhang L, Wang H, Liu Z, Zhang Z, Zheng Y. 2009. Differential expression of miRNAs in response to salt stress in maize roots. Annals of Botany 103, 29-38.
22. Ellis MH, Dennis ES, Peacock WJ. 1999. Arabidopsis roots and shoots have different mechanisms for hypoxic stress tolerance. Plant Physiology 119, 57-64.
23. Fahlgren N, Howell MD, Kasschau KD, et al. 2007. High-throughput sequencing of Arabidopsis microRNAs: evidence for frequent birth and death of MIRNA Genes. PLoS ONE 2, e219.
24. Fukao T, Xu KN, Ronald PC, Bailey-Serres J. 2006. A variable cluster of ethylene response factor-like genes regulates metabolic and developmental acclimation responses to submergence in rice. The Plant Cell 18, 2021-2034.
25. Ghildiyal M, Zamore PD. 2009. Small silencing RNAs: an expanding universe. Nature Reviews Genetics 10, 94-108.
26. Griffiths-Jones S. 2004. The microRNA registry. Nucleic Acids Research 32, D109-D111.
27. Gustafson AM, Allen E, Givan S, Smith D, Carrington JC, Kasschau KD. 2005. ASRP: the Arabidopsis Small RNA Project database. Nucleic Acids Research 33, D637-640.
28. Hattori Y, Nagai K, Furukawa S, et al. 2009. The ethylene response factors SNORKEL1 and SNORKEL2 allow rice to adapt to deep water. Nature 460, 1026-1030.
29. He CJ, Morgan PW, Drew MC. 1996. Transduction of an ethylene signal is required for cell death and lysis in the root cortex of maize during aerenchyma formation induced by hypoxia. Plant Physiology 112, 463-472.
30. Henriksson E, Olsson ASB, Johannesson H, Johansson H, Hanson J, Engstrom P, Soderman E. 2005. Homeodomain leucine zipper class I genes in Arabidopsis. Expression patterns and phylogenetic relationships. Plant Physiology 139, 509-518.
31. Hoeren FU, Dolferus R, Wu Y, Peacock WJ, Dennis ES. 1998. Evidence for a role for AtMYB2 in the induction of the Arabidopsis alcohol dehydrogenase gene (ADH1) by low oxygen. Genetics 149, 479-490.
32. Hunter C, Willmann MR, Wu G, Yoshikawa M, de la Luz Gutierrez-Nava M, Poethig RS. 2006. Trans-acting siRNA-mediated repression of ETTIN and ARF4 regulates heteroblasty in Arabidopsis. Development 133, 2973-2981.
33. Igamberdiev AU, Hill RD. 2009. Plant mitochondrial function during anaerobiosis. Annals of Botany 103, 259-268.
34. Ikuma H, Bonner WD. 1967. Properties of higher plant mitochondria. 3. Effects of respiratory inhibitors. Plant Physiology 42, 1535-1544.
35. Katiyar-Agarwal S, Morgan R, Dahlbeck D, Borsani O, Villegas Jr A, Zhu JK, Staskawicz BJ, Jin H. 2006. A pathogen-inducible endogenous siRNA in plant immunity. Proceedings of the National Academy of Sciences, USA 103, 18002-18007.
36. Klok EJ, Wilson IW, Wilson D, Chapman SC, Ewing RM, Somerville SC, Peacock WJ, Dolferus R, Dennis ES. 2002. Expression profile analysis of the low-oxygen response in Arabidopsis root cultures. The Plant Cell 14, 2481-2494.
37. Kreuzwieser J, Hauberg J, Howell KA, Carroll A, Rennenberg H, Millar AH, Whelan J. 2009. Differential response of grey poplar leaves and roots underpins stress adaptation during hypoxia. Plant Physiology 149, 461-473.
38. Lasanthi-Kudahettige R, Magneschi L, Loreti E, Gonzali S, Licausi F, Novi G, Beretta O, Vitulli F, Alpi A, Perata P. 2007. Transcript profiling of the anoxic rice coleoptile. Plant Physiology 144, 218-231.
39. Li RQ, Li YR, Kristiansen K, Wang J. 2008. SOAP: short oligonucleotide alignment program. Bioinformatics 24, 713-714.
40. Liu FL, VanToai T, Moy LP, Bock G, Linford LD, Quackenbush J. 2005. Global transcription profiling reveals comprehensive insights into hypoxic response in Arabidopsis. Plant Physiology 137, 1115-1129.
41. Loreti E, Poggi A, Novi G, Alpi A, Perata P. 2005. A genome-wide analysis of the effects of sucrose on gene expression in Arabidopsis seedlings under anoxia. Plant Physiology 137, 1130-1138.
42. Lu C, Meyers BC, Green PJ. 2007. Construction of small RNA cDNA libraries for deep sequencing. Methods 43, 110-117.
43. Lu SF, Sun YH, Chiang VL. 2008. Stress-responsive microRNAs in Populus. The Plant Journal 55, 131-151.
44. Lurin C, Andres C, Aubourg S, et al. 2004. Genome-wide analysis of Arabidopsis pentatricopeptide repeat proteins reveals their essential role in organelle biogenesis. The Plant Cell 16, 2089-2103.
45. Maizel A, Marin E, Herz A, Crespi M. 2008. Activation of the TAS3-derived tasiRNA pathway in the root system of Arabidopsis. Comparative Biochemistry and Physiology Part A, Molecular and Integrative Physiology 150, S197-S197.
46. Maxwell DP, Wang Y, McIntosh L. 1999. The alternative oxidase lowers mitochondrial reactive oxygen production in plant cells. Proceedings of the National Academy of Sciences, USA 96, 8271-8276.
47. Megraw M, Baev V, Rusinov V, Jensen ST, Kalantidis K, Hatzigeorgiou AG. 2006. MicroRNA promoter element discovery in Arabidopsis. RNA 12, 1612-1619.
48. Murashige T, Skoog F. 1962. A revised medium for rapid growth and bioassays with tobacco tissue culture. Physiologia Plantarum 15, 473-497.
49. Nobuta K, Lu C, Shrivastava R, et al. 2008. Distinct size distribution of endogenous siRNAs in maize: evidence from deep sequencing in the mop1-1 mutant. Proceedings of the National Academy of Sciences, USA 105, 14958-14963.
50. Qiu D, Pan X, Wilson IW, Li F, Liu M, Teng W, Zhang B. 2009. High throughput sequencing technology reveals that the taxoid elicitor methyl jasmonate regulates microRNA expression in Chinese yew (Taxus chinensis). Gene 436, 37-44.
51. Rajagopalan R, Vaucheret H, Trejo J, Bartel DP. 2006. A diverse and evolutionarily fluid set of microRNAs in Arabidopsis thaliana. Genes and Development 20, 3407-3425.
52. Reyes JL, Chua NH. 2007. ABA induction of miR159 controls transcript levels of two MYB factors during Arabidopsis seed germination. The Plant Journal 49, 592-606.
53. Rhee SY, Beavis W, Berardini TZ, et al. 2003. The Arabidopsis Information Resource (TAIR): a model organism database providing a centralized, curated gateway to Arabidopsis biology, research materials and community. Nucleic Acids Research 31, 224-228.
54. Rhoads DM, Subbaiah CC. 2007. Mitochondrial retrograde regulation in plants. Mitochondrion 7, 177-194.
55. Schonbaum GR, Bonner WD, Storey BT, Bahr JT. 1971. Specific inhibition of cyanide-insensitive respiratory pathway in plant mitochondria by hydroxamic acids. Plant Physiology 47, 124-128.
56. Schwarz S, Grande AV, Bujdoso N, Saedler H, Huijser P. 2008. The microRNA regulated SBP-box genes SPL9 and SPL15 control shoot maturation in Arabidopsis. Plant Molecular Biology 67, 183-195.
57. Semenza GL. 1999. Perspectives on oxygen sensing. Cell 98, 281-284.
58. Singh KB. 1998. Transcriptional regulation in plants: the importance of combinatorial control. Plant Physiology 118, 1111-1120.
59. Subbaiah CC, Bush DS, Sachs MM. 1994a. Elevation of cytosolic calcium precedes anoxic gene-expression in Maize suspension-cultured cells. The Plant Cell 6, 1747-1762.
60. Subbaiah CC, Sachs MM. 2003. Molecular and cellular adaptations of maize to flooding stress. Annals of Botany 91, 119-127.
61. Subbaiah CC, Zhang JK, Sachs MM. 1994b. Involvement of intracellular calcium in anaerobic gene-expression and survival of maize seedlings. Plant Physiology 105, 369-376.
62. Sunkar R, Chinnusamy V, Zhu J, Zhu JK. 2007. Small RNAs as big players in plant abiotic stress responses and nutrient deprivation. Trends in Plant Science 12, 301-309.
63. Sunkar R, Kapoor A, Zhu JK. 2006. Posttranscriptional induction of two Cu/Zn superoxide dismutase genes in Arabidopsis is mediated by downregulation of miR398 and important for oxidative stress tolerance. The Plant Cell 18, 2051-2065.
64. Sunkar R, Zhu JK. 2004. Novel and stress-regulated microRNAs and other small RNAs from Arabidopsis. The Plant Cell 16, 2001-2019.
65. Szittya G, Moxon S, Santos DM, Jing R, Fevereiro MPS, Moulton V, Dalmay T. 2008. High-throughput sequencing of Medicago truncatula short RNAs identifies eight new miRNA families. BMC Genomics 9, 593.
66. Tagami Y, Inaba N, Kurihara Y, Kutsuna N, Watanabe Y. 2007. Small RNA expression profile of Arabidopsis thaliana infected with tobacco mosaic virus. Plant and Cell Physiology 48, S36-S36.
67. Thoen PAC, Ariyurek Y, Thygesen HH, Vreugdenhil E, Vossen RHAM, de Menezes RX, Boer JM, van Ommen G-JB, den Dunnen JT. 2008. Deep sequencing-based expression analysis shows major advances in robustness, resolution and inter-lab portability over five microarray platforms. Nucleic Acids Research 36;e141.
68. Valoczi A, Varallyay E, Kauppinen S, Burgyan J, Havelda Z. 2006. Spatio-temporal accumulation of microRNAs is highly coordinated in developing plant tissues. The Plant Journal 47, 140-151.
69. Van Dongen JT, Frohlich A, Ramirez-Aguilar SJ, Schauer N, Fernie AR, Erban A, Kopka J, Clark J, Langer A, Geigenberger P. 2009. Transcript and metabolite profiling of the adaptive response to mild decreases in oxygen concentration in the roots of Arabidopsis plants. Annals of Botany 103, 269-280.
70. Varkonyi-Gasic E, Wu RM, Wood M, Walton EF, Hellens RP. 2007. Protocol: a highly sensitive RT-PCR method for detection and quantification of microRNAs. Plant Methods 3, 12.
71. Vazquez F. 2006. Arabidopsis endogenous small RNAs: highways and byways. Trends in Plant Science 11, 460-468.
72. Wilson IW, Kennedy GC, Peacock JW, Dennis ES. 2005. Microarray analysis reveals vegetative molecular phenotypes of arabidopsis flowering-time mutants. Plant and Cell Physiology 46, 1190-1201.
73. Xu K, Xu X, Fukao T, Canlas P, Maghirang-Rodriguez R, Heuer S, Ismail AM, Bailey-Serres J, Ronald PC, Mackill DJ. 2006. Sub1A is an ethylene-response- factor-like gene that confers submergence tolerance to rice. Nature 442, 705-708.
74. Zhang Z, Wei L, Zou X, Tao Y, Liu Z, Zheng Y. 2008. Submergence- responsive microRNAs are potentially involved in the regulation of morphological and metabolic adaptations in maize root cells. Annals of Botany 102, 509-519.
75. Zhou X, Wang G, Sutoh K, Zhu JK, Zhang W. 2008. Identification of cold-inducible microRNAs in plants by transcriptome analysis. Biochimica et Biophysica Acta 1779, 780-788.
76. Zhou XF, Ruan JH, Wang GD, Zhang WX. 2007. Characterization and identification of microRNA core promoters in four model species. PLos Computational Biology 3, 412-423.
77. Zhu QH, Spriggs A, Matthew L, Fan LJ, Kennedy G, Gubler F, Helliwell C. 2008. A diverse set of microRNAs and microRNA-like small RNAs in developing rice grains. Genome Research 18, 1456-1465.
78. Zimmermann P, Hirsch-Hoffmann M, Hennig L, Gruissem W. 2004. GENEVESTIGATOR. Arabidopsis microarray database and analysis toolbox. Plant Physiology 136, 2621-2632.