A gain-of-function mutation in IAA16 confers reduced responses to auxin and abscisic acid and impedes plant growth and fertility

Plant Molecular Biology

Volumn 79, Issue 4-5, 2012, Pages 359-373

  Rinaldi, Mauro A ^b   Liu, James ^b,c   Enders, Tara A ^a   Bartel, Bonnie ^b   Strader, Lucia C ^a  

^a WASHINGTON UNIVERSITY   (United States)

^b RICE UNIVERSITY   (United States)

^c Epic   (United States)

Author keywords

Abscisic acid; Aux IAA gain of function; Auxin signaling; IAA16

Indexed keywords

ABSCISIC ACID; ARABIDOPSIS PROTEIN; INDOLEACETIC ACID DERIVATIVE; PHYTOHORMONE; PLANT DNA;

AMINO ACID SEQUENCE; ARABIDOPSIS; ARTICLE; DRUG EFFECT; FERTILITY; GENETICS; GROWTH, DEVELOPMENT AND AGING; MOLECULAR GENETICS; MULTIGENE FAMILY; MUTATION; NUCLEOTIDE SEQUENCE; PHENOTYPE; PHYLOGENY; PHYSIOLOGY; PLANT GENE; PLANT ROOT; SEQUENCE HOMOLOGY; SIGNAL TRANSDUCTION;

ABSCISIC ACID; AMINO ACID SEQUENCE; ARABIDOPSIS; ARABIDOPSIS PROTEINS; BASE SEQUENCE; DNA, PLANT; FERTILITY; GENES, PLANT; INDOLEACETIC ACIDS; MOLECULAR SEQUENCE DATA; MULTIGENE FAMILY; MUTATION; PHENOTYPE; PHYLOGENY; PLANT GROWTH REGULATORS; PLANT ROOTS; SEQUENCE HOMOLOGY, AMINO ACID; SIGNAL TRANSDUCTION;

ARABIDOPSIS; ARABIDOPSIS THALIANA;

EID: 84862010930     PISSN: 01674412     EISSN: None     Source Type: Journal    
DOI: 10.1007/s11103-012-9917-y     Document Type: Article

References (79)

1. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215: 403-410.
2. Beaudoin N, Serizet C, Gosti F, Giraudat J (2000) Interactions between abscisic acid and ethylene signaling cascades. Plant Cell 12: 1103-1115.
3. Belin C, Megies C, Hauserova E, Lopez-Molina L (2009) Abscisic acid represses growth of the Arabidopsis embryonic axis after germination by enhancing auxin signaling. Plant Cell 21: 2253-2268.
4. Bell CJ, Ecker JR (1994) Assignment of 30 microsatellite loci to the linkage map of Arabidopsis. Genomics 19: 137-144.
5. Brady SM, Sarkar SF, Bonetta D, McCourt P (2003) The ABSCISIC ACID INSENSITIVE 3 (ABI3) gene is modulated by farnesylation and is involved in auxin signaling and lateral root development in Arabidopsis. Plant J 34: 67-75.
6. Calderon-Villalobos LI, Tan X, Zheng N, Estelle M (2010) Auxin perception-structural insights. Cold Spring Harb Perspect Biol 2: a005546.
7. Celenza JL, Grisafi PL, Fink GR (1995) A pathway for lateral root formation in Arabidopsisthaliana. Genes Dev 9: 2131-2142.
8. Che P, Gingerich DJ, Lall S, Howell SH (2002) Global and hormone-induced gene expression changes during shoot development in Arabidopsis. Plant Cell 14: 2771-2785.
9. Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16: 735-743.
10. Curtis MD, Grossniklaus U (2003) A gateway cloning vector set for high-throughput functional analysis of genes in planta. Plant Physiol 133: 462-469.
11. Cutler S, Ghassemian M, Bonetta D, Cooney S, McCourt P (1996) A protein farnesyl transferase involved in abscisic acid signal transduction in Arabidopsis. Science 273: 1239-1241.
12. Dharmasiri N, Dharmasiri S, Estelle M (2005a) The F-box protein TIR1 is an auxin receptor. Nature 435: 441-445.
13. Dharmasiri N, Dharmasiri S, Weijers D, Lechner E, Yamada M, Hobbie L, Ehrismann JS, Jürgens G, Estelle M (2005b) Plant development is regulated by a family of auxin receptor F box proteins. Dev Cell 9: 109-119.
14. dos Santos Maraschin F, Memelink J, Offringa R (2009) Auxin-induced, SCF(TIR1)-mediated poly-ubiquitination marks AUX/IAA proteins for degradation. Plant J 59: 100-109.
15. Dreher KA, Brown J, Saw RE, Callis J (2006) The Arabidopsis Aux/IAA protein family has diversified in degradation and auxin responsiveness. Plant Cell 18: 699-714.
16. Finkelstein RR (1994) Maternal effects govern variable dominance of two abscisic acid response mutations in Arabidopsis thaliana. Plant Physiol 105: 1203-1208.
17. Friml J, Wiśniewska J, Benková E, Mendgen K, Palme K (2002) Lateral relocation of auxin efflux regulator PIN3 mediates tropism in Arabidopsis. Nature 415: 806-809.
18. Fukaki H, Tameda S, Masuda H, Tasaka M (2002) Lateral root formation is blocked by a gain-of-function mutation in the SOLITARY-ROOT/IAA14 gene of Arabidopsis. Plant J 29: 153-168.
19. Goda H, Sawa S, Asami T, Fujioka S, Shimada Y, Yoshida S (2004) Comprehensive comparison of auxin-regulated and brassinosteroid-regulated genes in Arabidopsis. Plant Physiol 134: 1555-1573.
20. Gray WM, Östin A, Sandberg G, Romano CP, Estelle M (1998) High temperature promotes auxin-mediated hypocotyl elongation in Arabidopsis. Proc Natl Acad Sci USA 95: 7197-7202.
21. Grierson C, Schiefelbein J (2002) Root hairs: April 4, 2002. In: The Arabidopsis Book. American Society of Plant Biologists, Rockville, p 1: e0060.
22. Guilfoyle TJ, Hagen G (2007) Auxin response factors. Curr Opin Plant Biol 10: 453-460.
23. Hagen G, Guilfoyle T (2002) Auxin-responsive gene expression: genes, promoters and regulatory factors. Plant Mol Biol 49: 373-385.
24. Hamann T, Mayer U, Jürgens G (1999) The auxin-insensitive bodenlos mutation affects primary root formation and apical-basal patterning in the Arabidopsis embryo. Development 126: 1387-1395.
25. Hamann T, Benkova E, Bäurle I, Kientz M, Jürgens G (2002) The Arabidopsis BODENLOS gene encodes an auxin response protein inhibiting MONOPTEROS-mediated embryo patterning. Genes Dev 16: 1610-1615.
26. Haughn GW, Somerville C (1986) Sulfonylurea-resistant mutants of Arabidopsis thaliana. Mol Gen Genet 204: 430-434.
27. Himmelbach A, Iten M, Grill E (1998) Signalling of abscisic acid to regulate plant growth. Philos Trans R Soc Lond B Biol Sci 353: 1439-1444.
28. TIR1 complex. Proc Natl Acad Sci USA 101: 12381-12386.
29. Kepinski S, Leyser O (2005) The Arabidopsis F-box protein TIR1 is an auxin receptor. Nature 435: 446-451.
30. Kim BC, Soh MS, Kang BJ, Furuya M, Nam HG (1996) Two dominant photomorphogenic mutations of Arabidopsis thaliana identified as suppressor mutations of hy2. Plant J 9: 441-456.
31. Kim J, Harter K, Theologis A (1997) Protein-protein interactions among the Aux/IAA proteins. Proc Natl Acad Sci USA 94: 11786-11791.
32. Kim BC, Soh MS, Hong SH, Furuya M, Nam HG (1998) Photomorphogenic development of the Arabidopsis shy2-1D mutation and its interaction with phytochromes in darkness. Plant J 15: 61-68.
33. Knox K, Grierson CS, Leyser O (2003) AXR3 and SHY2 interact to regulate root hair development. Development 130: 5769-5777.
34. L-DNA gene 5 controls the tissue-specific expression of chimaeric genes carried by a novel type of Agrobacterium binary vector. Mol Gen Genet 204: 383-396.
35. Konieczny A, Ausubel FM (1993) A procedure for mapping Arabidopsis mutations using co-dominant ecotype-specific PCR-based markers. Plant J 4: 403-410.
36. Koornneef M, Reuling G, Karssen CM (1984) The isolation and characterization of abscisic acid-insensitive mutants of Arabidopsis thaliana. Physiol Plant 61: 377-383.
37. Kwak JM, Moon JH, Murata Y, Kuchitsu K, Leonhardt N, DeLong A, Schroeder JI (2002) Disruption of a guard cell-expressed protein phosphatase 2A regulatory subunit, RCN1, confers abscisic acid insensitivity in Arabidopsis. Plant Cell 14: 2849-2861.
38. Leyser HMO, Pickett FB, Dharmasiri S, Estelle M (1996) Mutations in the AXR3 gene of Arabidopsis result in altered auxin response including ectopic expression from the SAUR-AC1 promoter. Plant J 10: 403-413.
39. Li H, Tiwari SB, Hagen G, Guilfoyle TJ (2011) Identical amino acid substitutions in the repression domain of auxin/indole-3-acetic acid proteins have contrasting effects on auxin signaling. Plant Physiol 155: 1252-1263.
40. Liscum E, Reed JW (2002) Genetics of Aux/IAA and ARF action in plant growth and development. Plant Mol Biol 49: 387-400.
41. Maher EP, Martindale SJB (1980) Mutants of Arabidopsis thaliana with altered responses to auxins and gravity. Biochem Genet 18: 1041-1053.
42. Masson PH (1995) Root gravitropism. BioEssays News Rev Mol cell Dev Biol 17: 119-127.
43. Mockaitis K, Estelle M (2008) Auxin receptors and plant development: a new signaling paradigm. Annu Rev Cell Dev Biol 24: 55-80.
44. Monroe-Augustus M, Zolman BK, Bartel B (2003) IBR5, a dual-specificity phosphatase-like protein modulating auxin and abscisic acid responsiveness in Arabidopsis. Plant Cell 15: 2979-2991.
45. Muto H, Watahiki MK, Nakamoto D, Kinjo M, Yamamoto KT (2007) Specificity and similarity of functions of the Aux/IAA genes in auxin signaling of Arabidopsis revealed by promoter-exchange experiments among MSG2/IAA19, AXR2/IAA7, and SLR/IAA14. Plant Physiol 144: 187-196.
46. Nagpal P, Walker LM, Young JC, Sonawala A, Timpte C, Estelle M, Reed JW (2000) AXR2 encodes a member of the Aux/IAA protein family. Plant Physiol 123: 563-573.
47. Ouellet F, Overvoorde PJ, Theologis A (2001) IAA17/AXR3: biochemical insight into an auxin mutant phenotype. Plant Cell 13: 829-841.
48. Overvoorde PJ, Okushima Y, Alonso JM, Chan A, Chang C, Ecker JR, Hughes B, Liu A, Onodera C, Quach H, Smith A, Yu G, Theologis A (2005) Functional genomic analysis of the AUXIN/INDOLE-3-ACETIC ACID gene family members in Arabidopsis thaliana. Plant Cell 17: 3282-3300.
49. Perrot-Rechenmann C (2010) Cellular responses to auxin: division versus expansion. Cold Spring Harb Perspect Biol 2: a001446.
50. Prigge MJ, Lavy M, Ashton NW, Estelle M (2010) Physcomitrella patens auxin-resistant mutants affect conserved elements of an auxin-signaling pathway. Curr Biol 20: 1907-1912.
51. Ramos JA, Zenser N, Leyser O, Callis J (2001) Rapid degradation of auxin/indoleacetic acid proteins requires conserved amino acids of domain II and is proteasome dependent. Plant Cell 13: 2349-2360.
52. Reed JW, Elumalai RP, Chory J (1998) Suppressors of an Arabidopsis thaliana phyB mutation identify genes that control light signaling and hypocotyl elongation. Genetics 148: 1295-1310.
53. Remington DL, Vision TJ, Guilfoyle TJ, Reed JW (2004) Contrasting modes of diversification in the Aux/IAA and ARF gene families. Plant Physiol 135: 1738-1752.
54. Rock CD, Sun X (2005) Crosstalk between ABA and auxin signaling pathways in roots of Arabidopsis thaliana (L.) Heynh. Planta 222: 98-106.
55. Rogg LE (2001) Cloning and characterization of IAA28, a gene involved in suppressing lateral root development and mediating auxin responses in Arabidopsis thaliana. Rice University, Houston, PhD.
56. Rogg LE, Lasswell J, Bartel B (2001) A gain-of-function mutation in IAA28 suppresses lateral root development. Plant Cell 13: 465-480.
57. Rouse D, Mackay P, Stirnberg P, Estelle M, Leyser O (1998) Changes in auxin response from mutations in an AUX/IAA gene. Science 279: 1371-1373.
58. Schmid M, Davison TS, Henz SR, Pape UJ, Demar M, Vingron M, Scholkopf B, Weigel D, Lohmann JU (2005) A gene expression map of Arabidopsis thaliana development. Nat Genet 37: 501-506.
59. Stasinopoulos TC, Hangarter RP (1990) Preventing photochemistry in culture media by long-pass light filters alters growth of cultured tissues. Plant Physiol 93: 1365-1369.
60. Strader LC, Monroe-Augustus M, Bartel B (2008a) The IBR5 phosphatase promotes Arabidopsis auxin responses through a novel mechanism distinct from TIR1-mediated repressor degradation. BMC Plant Biol 8: 41.
61. Strader LC, Monroe-Augustus M, Rogers KC, Lin GL, Bartel B (2008b) Arabidopsis iba response5 (ibr5) suppressors separate responses to various hormones. Genetics 180: 2019-2031.
62. Sundberg E, Ostergaard L (2009) Distinct and dynamic auxin activities during reproductive development. Cold Spring Harb Perspect Biol 1: a001628.
63. Swofford DL (2001) PAUP*. Phylogenetic analysis using parsimony (and other methods), 4th edn. Sinauer Associates, Sunderland.
64. Szemenyei H, Hannon M, Long JA (2008) TOPLESS mediates auxin-dependent transcriptional repression during Arabidopsis embryogenesis. Science 319: 1384-1386.
65. Tan X, Calderon-Villalobos LI, Sharon M, Zheng C, Robinson CV, Estelle M, Zheng N (2007) Mechanism of auxin perception by the TIR1 ubiquitin ligase. Nature 446: 640-645.
66. Tatematsu K, Kumagai S, Muto H, Sato A, Watahiki MK, Harper RM, Liscum E, Yamamoto KT (2004) MASSUGU2 encodes Aux/IAA19, an auxin-regulated protein that functions together with the transcriptional activator NPH4/ARF7 to regulate differential growth responses of hypocotyl and formation of lateral roots in Arabidopsis thaliana. Plant Cell 16: 379-393.
67. Tian Q, Reed JW (1999) Control of auxin-regulated root development by the Arabidopsis thaliana SHY2/IAA3 gene. Development 126: 711-721.
68. Timpte C, Wilson AK, Estelle M (1994) The axr2-1 mutation of Arabidopsis thaliana is a gain-of-function mutation that disrupts an early step in auxin response. Genetics 138: 1239-1249.
69. Uehara T, Okushima Y, Mimura T, Tasaka M, Fukaki H (2008) Domain II mutations in CRANE/IAA18 suppress lateral root formation and affect shoot development in Arabidopsis thaliana. Plant Cell Physiol 49: 1025-1038.
70. Ulmasov T, Murfett J, Hagen G, Guilfoyle TJ (1997) Aux/IAA proteins repress expression of reporter genes containing natural and highly active synthetic auxin response elements. Plant Cell 9: 1963-1971.
71. Vandenbussche F, Petrášek J, Žádníková P, Hoyerová K, Pešek B, Raz V, Swarup R, Bennett M, Zažímalová E, Benková E, van Der Straeten D (2010) The auxin influx carriers AUX1 and LAX3 are involved in auxin-ethylene interactions during apical hook development in Arabidopsis thaliana seedlings. Development 137: 597-606.
72. Vernoux T, Brunoud G, Farcot E, Morin V, van den Daele H, Legrand J, Oliva M, Das P, Larrieu A, Wells D, Guedon Y, Armitage L, Picard F, Guyomarc'h S, Cellier C, Parry G, Koumproglou R, Doonan JH, Estelle M, Godin C, Kepinski S, Bennett M, De Veylder L, Traas J (2011) The auxin signalling network translates dynamic input into robust patterning at the shoot apex. Mol Syst Biol 7: 508.
73. Wasilewska A, Vlad F, Sirichandra C, Redko Y, Jammes F, Valon C, Frei dit Frey N, Leung J (2008) An update on abscisic acid signaling in plants and more. Mol Plant 1: 198-217.
74. Weijers D, Benkova E, Jager KE, Schlereth A, Hamann T, Kientz M, Wilmoth JC, Reed JW, Jurgens G (2005) Developmental specificity of auxin response by pairs of ARF and Aux/IAA transcriptional regulators. EMBO J 24: 1874-1885.
75. Wilson AK, Pickett FB, Turner JC, Estelle M (1990) A dominant mutation in Arabidopsis confers resistance to auxin, ethylene, and abscisic acid. Mol Gen Genet 222: 377-383.
76. Winter D, Vinegar B, Nahal H, Ammar R, Wilson GV, Provart NJ (2007) An "electronic fluorescent pictograph" browser for exploring and analyzing large-scale biological data sets. PLoS ONE 2: e718.
77. Worley CK, Zenser N, Ramos J, Rouse D, Leyser O, Theologis A, Callis J (2000) Degradation of Aux/IAA proteins is essential for normal auxin signalling. Plant J 21: 553-562.
78. TIR1. Plant J 40: 772-782.
79. Žádníková P, Petrášek J, Marhavý P, Raz V, Vandenbussche F, Ding Z, Schwarzerová K, Morita MT, Tasaka M, Hejátko J, van Der Straeten D, Friml J, Benková E (2010) Role of PIN-mediated auxin efflux in apical hook development of Arabidopsis thaliana. Development 137: 607-617.