Modifications of a conserved regulatory network involving INDEHISCENT controls multiple aspects of reproductive tissue development in Arabidopsis

New Phytologist

Volumn 197, Issue 1, 2013, Pages 73-87

  Kay, P ^a,b   Groszmann, M ^a   Ross, J J ^c   Parish, R W ^b   Swain, S M ^a  

^a CSIRO   (Australia)

^b LA TROBE UNIVERSITY   (Australia)

^c UNIVERSITY OF TASMANIA   (Australia)

Author keywords

Anther and pollen; Arabidopsis reproductive development; Auxin; Gibberellin (GA); HECATE; INDEHISCENT; SHATTERPROOF; Valve margin

Indexed keywords

ALCATRAZ PROTEIN, ARABIDOPSIS; ARABIDOPSIS PROTEIN; ARGININE; BASIC HELIX LOOP HELIX TRANSCRIPTION FACTOR; GIBBERELLIC ACID; GIBBERELLIN; INDEHISCENT PROTEIN, ARABIDOPSIS; INDOLEACETIC ACID DERIVATIVE; MADS DOMAIN PROTEIN; SHP1 PROTEIN, ARABIDOPSIS; SHP2 PROTEIN, ARABIDOPSIS;

ALLELE; BIOLOGICAL DEVELOPMENT; DICOTYLEDON; FRUITING; FUNCTIONAL ROLE; GENE EXPRESSION; GROWTH REGULATOR; HORMONE; PHYTOCHEMISTRY; POLLEN; PROTEIN; REPRODUCTIVE BIOLOGY; SEED SET;

ALLELE; ARABIDOPSIS; ARTICLE; FERTILITY; GENE EXPRESSION REGULATION; GENE REGULATORY NETWORK; GENETIC TRANSCRIPTION; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; PHYLOGENY; PLANT GENE; PLANT SEED; POLLEN TUBE; POLLINATION; PROTEIN STABILITY; REPRODUCTION; SELF FERTILIZATION; TRANSGENIC PLANT;

ALLELES; ARABIDOPSIS; ARABIDOPSIS PROTEINS; ARGININE; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; FERTILITY; GENE EXPRESSION REGULATION, PLANT; GENE REGULATORY NETWORKS; GENES, PLANT; GIBBERELLINS; INDOLEACETIC ACIDS; MADS DOMAIN PROTEINS; PHYLOGENY; PLANTS, GENETICALLY MODIFIED; POLLEN TUBE; POLLINATION; PROTEIN STABILITY; REPRODUCTION; SEEDS; SELF-FERTILIZATION; TRANSCRIPTION, GENETIC;

ARABIDOPSIS;

EID: 84870187082     PISSN: 0028646X     EISSN: 14698137     Source Type: Journal    
DOI: 10.1111/j.1469-8137.2012.04373.x     Document Type: Article

References (75)

1. Aloni R, Aloni E, Langhans M, Ullrich CI. 2006. Role of auxin in regulating Arabidopsis flower development. Planta 223: 315-328.
2. Alvarez J, Smyth DR. 2002. CRABS CLAW and SPATULA genes regulate growth and pattern formation during gynoecium development in Arabidopsis thaliana. International Journal of Plant Sciences 163: 17-41.
3. Arnaud N, Girin T, Sorefan K, Fuentes S, Wood TA, Lawrenson T, Sablowski R, Ostergaard L. 2010. Gibberellins control fruit patterning in Arabidopsis thaliana. Genes & Development 24: 2127-2132.
4. Bailey PC, Martin C, Toledo-Ortiz G, Quail PH, Huq E, Heim MA, Jakoby M, Werber M, Weisshaar B. 2003. Update on the basic helix-loop-helix transcription factor gene family in Arabidopsis thaliana. Plant Cell 15: 2497-2501.
5. Benjamins R, Quint A, Weijers D, Hooykaas P, Offringa R. 2001. The PINOID protein kinase regulates organ development in Arabidopsis by enhancing polar auxin transport. Development 128: 4057-4067.
6. Blanc G, Hokamp K, Wolfe KH. 2003. A recent polyploidy superimposed on older large-scale duplications in the Arabidopsis genome. Genome Research 13: 137-144.
7. Cecchetti V, Altamura MM, Falasca G, Costantino P, Cardarelli M. 2008. Auxin regulates Arabidopsis anther dehiscence, pollen maturation, and filament elongation. Plant Cell 20: 1760-1774.
8. Chapman EJ, Greenham K, Castillejo C, Sartor R, Bialy A, Sun TP, Estelle M. 2012. Hypocotyl transcriptome reveals auxin regulation of growth-promoting genes through GA-dependent and -independent pathways. PLoS ONE 7: e36210.
9. Cheng Y, Dai X, Zhao Y. 2007. Auxin synthesized by the YUCCA flavin monooxygenases is essential for embryogenesis and leaf formation in Arabidopsis. Plant Cell 19: 2430-2439.
10. Cheng YF, Dai XH, Zhao YD. 2006. Auxin biosynthesis by the YUCCA flavin monooxygenases controls the formation of floral organs and vascular tissues in Arabidopsis. Genes & Development 20: 1790-1799.
11. Colombo M, Brambilla V, Marcheselli R, Caporali E, Kater MM, Colombo L. 2010. A new role for the SHATTERPROOF genes during Arabidopsis gynoecium development. Developmental Biology 337: 294-302.
12. Cox CM, Swain SM. 2006. Localised and non-localised promotion of fruit development by seeds in Arabidopsis. Functional Plant Biology 33: 1-8.
13. Depuydt S, Hardtke CS. 2011. Hormone signalling crosstalk in plant growth regulation. Current Biology 21: R365-R373.
14. Desgagne-Penix I, Sponsel VM. 2008. Expression of GIBBERELLIN 20-OXIDASE1 (AtGA20OX1) in Arabidopsis seedlings with altered auxin status is regulated at multiple levels. Journal of Experimental Botany 59: 2057-2070.
15. Dill A, Jun H-S, Sun TP. 2001. The DELLA motif is essential for gibberellin-induced degradation of RGA. Proceedings of the National Academy of Sciences 98: 14162-14167.
16. Dill A, Thomas SG, Hu JH, Steber CM, Sun TP. 2004. The Arabidopsis F-box protein SLEEPY1 targets gibberellin signaling repressors for gibberellin-induced degradation. Plant Cell 16: 1392-1405.
17. Dorcey E, Urbez C, Blázquez MA, Carbonell J, Perez-Amador MA. 2009. Fertilization-dependent auxin response in ovules triggers fruit development through the modulation of gibberellin metabolism in Arabidopsis. Plant Journal 58: 318-332.
18. Ferrandiz C, Liljegren SJ, Yanofsky MF. 2000. Negative regulation of the SHATTERPROOF genes by FRUITFULL during Arabidopsis fruit development. Science 289: 436-438.
19. Franzke A, Lysak MA, Al-Shehbaz IA, Koch MA, Mummenhoff K. 2011. Cabbage family affairs: the evolutionary history of Brassicaceae. Trends in Plant Science 16: 108-116.
20. Fu XD, Harberd NP. 2003. Auxin promotes Arabidopsis root growth by modulating gibberellin response. Nature 421: 740-743.
21. Gallego-Bartolome J, Minguet EG, Marin JA, Prat S, Blazquez MA, Alabadi D. 2010. Transcriptional diversification and functional conservation between DELLA proteins in Arabidopsis. Molecular Biology and Evolution 27: 1247-1256.
22. Girin T, Paicu T, Fuentes S, O'Brien M, Sorefan K, Stephenson P, Wood TA, Balanza V, Ferrandiz C, Smyth DR et al. 2011. INDEHISCENT and SPATULA interact to specify carpel and valve margin tissue and thus promote seed dispersal in Arabidopsis. The Plant Cell 23: 3641-3653.
23. Girin T, Stephenson P, Goldsack CM, Kempin SA, Perez A, Pires N, Sparrow PA, Wood TA, Yanofsky MF, Østergaard L. 2010. Brassicaceae INDEHISCENT genes specify valve margin cell fate and repress replum formation. Plant Journal 63: 329-338.
24. Goetz M, Hooper LC, Johnson SD, Rodrigues JCM, Vivian-Smith A, Koltunow AM. 2007. Expression of aberrant forms of AUXIN RESPONSE FACTOR8 stimulates parthenocarpy in Arabidopsis and tomato. Plant Physiology 145: 351-366.
25. Goetz M, Vivian-Smith A, Johnson SD, Koltunow AM. 2006. AUXIN RESPONSE FACTOR8 is a negative regulator of fruit initiation in Arabidopsis. Plant Cell 18: 1873-1886.
26. Gomi K, Sasaki A, Itoh H, Ueguchi-Tanaka M, Ashikari M, Kitano H, Matsuoka M. 2004. GID2, an F-box subunit of the SCF E3 complex, specifically interacts with phosphorylated SLR1 protein and regulates the gibberellin-dependent degradation of SLR1 in rice. Plant Journal 37: 626-634.
27. Gremski K, Ditta G, Yanofsky MF. 2007. The HECATE genes regulate female reproductive tract development in Arabidopsis thaliana. Development 134: 3593-3601.
28. Griffiths J, Murase K, Rieu I, Zentella R, Zhang Z-L, Powers SJ, Gong F, Phillips AL, Hedden P, Sun T-p et al. 2006. Genetic characterization and functional analysis of the GID1 gibberellin receptors in Arabidopsis. Plant Cell 18: 3399-3414.
29. Groszmann M, Bylstra Y, Lampugnani ER, Smyth DR. 2010. Regulation of tissue-specific expression of SPATULA, a bHLH gene involved in carpel development, seedling germination, and lateral organ growth in Arabidopsis. Journal of Experimental Botany 61: 1495-1508.
30. Groszmann M, Paicu T, Alvarez JP, Swain SM, Smyth DR. 2011. SPATULA and ALCATRAZ are partially redundant, functionally diverging bHLH genes required for Arabidopsis gynoecium and fruit development. The Plant Journal 68: 816-829.
31. Groszmann M, Paicu T, Smyth DR. 2008. Functional domains of SPATULA, a bHLH transcription factor involved in carpel and fruit development in Arabidopsis. Plant Journal 55: 40-52.
32. Guilfoyle TJ, Hagen G. 2007. Auxin response factors. Current Opinion in Plant Biology 10: 453-460.
33. Hedden P. 2003. The genes of the Green Revolution. Trends in Genetics 19: 5-9.
34. Heim MA, Jakoby M, Werber M, Martin C, Weisshaar B, Bailey PC. 2003. The basic helix-loop-helix transcription factor family in plants: a genome-wide study of protein structure and functional diversity. Molecular Biology and Evolution 20: 735-747.
35. Heslop-Harrison J, Heslop-Harrison Y. 1970. Evaluation of pollen viability by enzymatically induced fluorescence; intracellular hydrolysis of fluorescein diacetate. Stain Technology 45: 115-120.
36. Hu J, Mitchum MG, Barnaby N, Ayele BT, Ogawa M, Nam E, Lai W-C, Hanada A, Alonso JM, Ecker Jr. et al. 2008. Potential sites of bioactive gibberellin production during reproductive growth in Arabidopsis. Plant Cell 20: 320-336.
37. Ichihashi Y, Horiguchi G, Gleissberg S, Tsukaya H. 2010. The bHLH transcription factor SPATULA controls final leaf size in Arabidopsis thaliana. Plant and Cell Physiology 51: 252-261.
38. Itoh H, Matsuoka M, Steber CM. 2003. A role for the ubiquitin-26S-proteasome pathway in gibberellin signaling. Trends in Plant Science 8: 492-497.
39. Jiang LX, Yang SL, Xie LF, Puah CS, Zhang XQ, Yang WC, Sundaresan V, Ye D. 2005. VANGUARD1 encodes a pectin methylesterase that enhances pollen tube growth in the Arabidopsis style and transmitting tract. Plant Cell 17: 584-596.
40. Josse E-M, Gan Y, Bou-Torrent J, Stewart KL, Gilday AD, Jeffree CE, Vaistij FE, Martínez-García JF, Nagy F, Graham IA et al. 2011. A DELLA in disguise: SPATULA restrains the growth of the developing Arabidopsis seedling. Plant Cell 23: 1337-1351.
41. Larsson E, Sitbon F, Ljung K, von Arnold S. 2008. Inhibited polar auxin transport results in aberrant embryo development in Norway spruce. New Phytologist 177: 356-366.
42. Liljegren SJ, Ditta GS, Eshed HY, Savidge B, Bowman JL, Yanofsky MF. 2000. SHATTERPROOF MADS-box genes control seed dispersal in Arabidopsis. Nature 404: 766-770.
43. Liljegren SJ, Roeder AHK, Kempin SA, Gremski K, Ostergaard L, Guimil S, Reyes DK, Yanofsky MF. 2004. Control of fruit patterning in Arabidopsis by INDEHISCENT. Cell 116: 843-853.
44. Lukowitz W, Gillmor CS, Scheible WR. 2000. Positional cloning in arabidopsis. Why it feels good to have a genome initiative working for you. Plant Physiology 123: 795-805.
45. Lynch M, Conery JS. 2003. The evolutionary demography of duplicate genes. Journal of Structural and Functional Genomics 3: 35-44.
46. McGinnis KM, Thomas SG, Soule JD, Strader LC, Zale JM, Sun TP, Steber CM. 2003. The Arabidopsis SLEEPY1 gene encodes a putative F-box subunit of an SCF E3 ubiquitin ligase. Plant Cell 15: 1120-1130.
47. Nagpal P, Ellis CM, Weber H, Ploense SE, Barkawi LS, Guilfoyle TJ, Hagen G, Alonso JM, Cohen JD, Farmer EE et al. 2005. Auxin response factors ARF6 and ARF8 promote jasmonic acid production and flower maturation. Development 132: 4107-4118.
48. Nemhauser JL, Feldman LJ, Zambryski PC. 2000. Auxin and ETTIN in Arabidopsis gynoecium morphogenesis. Development 127: 3877-3888.
49. Ogawa M, Kay P, Wilson S, Swain SM. 2009. ARABIDOPSIS DEHISCENCE ZONE POLYGALACTURONASE1 (ADPG1), ADPG2, and QUARTET2 are polygalacturonases required for cell separation during reproductive development in Arabidopsis. Plant Cell 21: 216-233.
50. Okada K, Ueda J, Komaki MK, Bell CJ, Shimura Y. 1991. Requirement of the auxin polar transport-system in early stages of Arabidopsis floral bud formation. Plant Cell 3: 677-684.
51. Ostergaard L. 2009. Don't 'leaf' now. The making of a fruit. Current Opinion in Plant Biology 12: 36-41.
52. Ozga JA, van Huizen R, Reinecke DM. 2002. Hormone and seed-specific regulation of pea fruit growth. Plant Physiology 128: 1379-1389.
53. Palanivelu R, Brass L, Edlund AF, Preuss D. 2003. Pollen tube growth and guidance is regulated by POP2, an Arabidopsis gene that controls GABA levels. Cell 114: 47-59.
54. Penfield S, Josse E, Kannangara R, Gilday AD, Halliday KAnd, Graham IA. 2005. Cold and light control seed germination through the bHLH transcription factor SPATULA. Current Biology 15: 1998-2006.
55. Peng JR, Carol P, Richards DE, King KE, Cowling RJ, Murphy GP, Harberd NP. 1997. The Arabidopsis GAI gene defines a signaling pathway that negatively regulates gibberellin responses. Genes & Development 11: 3194-3205.
56. Pinyopich A, Ditta GS, Savidge B, Liljegren SJ, Baumann E, Wisman E, Yanofsky MF. 2003. Assessing the redundancy of MADS-box genes during carpel and ovule development. Nature 424: 85-88.
57. Rajani S, Sundaresan V. 2001. The Arabidopsis myc/bHLH gene ALCATRAZ enables cell separation in fruit dehiscence. Current Biology 11: 1914-1922.
58. Ross JJ, Weston DE, Davidson SE, Reid JB. 2011. Plant hormone interactions: how complex are they? Physiol. Plant 141: 299-309.
59. 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. Nature Genetics 37: 501-506.
60. Singh DP, Jermakow AM, Swain SM. 2002. Gibberellins are required for seed development and pollen tube growth in Arabidopsis. Plant Cell 14: 3133-3147.
61. Sorefan K, Girin T, Liljegren SJ, Ljung K, Robles P, Galvan-Ampudia CS, Offringa R, Friml J, Yanofsky MF, Ostergaard L. 2009. A regulated auxin minimum is required for seed dispersal in Arabidopsis. Nature 459: 583-586.
62. Sun T-p. 2011. The molecular mechanism and evolution of the GA-GID1-DELLA signaling module in plants. Current Biology 21: R338-R345.
63. Swain SM, Muller AJ, Singh DP. 2004. The gar2 and rga alleles increase the growth of gibberellin-deficient pollen tubes in Arabidopsis. Plant Physiology 134: 694-705.
64. Swain SM, Singh DP. 2005. Tall tales from sly dwarves: novel functions of gibberellins in plant development. Trends in Plant Science 10: 123-129.
65. Todesco M, Rubio-Somoza I, Paz-Ares J, Weigel D. 2010. A collection of target mimics for comprehensive analysis of microRNA function in Arabidopsis thaliana. PLoS Genetics 6: e1001031.
66. Toledo-Ortiz G, Huq E, Quail PH. 2003. The Arabidopsis basic/helix-loop-helix transcription factor family. Plant Cell 15: 1749-1770.
67. Ueguchi-Tanaka M, Ashikari M, Nakajima M, Itoh H, Katoh E, Kobayashi M, Chow TY, Hsing YIC, Kitano H, Yamaguchi I et al. 2005. GIBBERELLIN INSENSITIVE DWARF1 encodes a soluble receptor for gibberellin. Nature 437: 693-698.
68. Ueguchi-Tanaka M, Nakajima M, Katoh E, Ohmiya H, Asano K, Saji S, Xiang H, Ashikari M, Kitano H, Yamaguchi I et al. 2007. Molecular interactions of a soluble gibberellin receptor, GID1, with a rice DELLA protein, SLR1, and gibberellin. Plant Cell 19: 2140-2155.
69. Vanneste S, Friml J. 2009. Auxin: a trigger for change in plant development. Cell 136: 1005-1016.
70. Vivian-Smith A, Luo M, Chaudhury A, Koltunow A. 2001. Fruit development is actively restricted in the absence of fertilization in Arabidopsis. Development 128: 2321-2331.
71. Wagner A. 1998. The fate of duplicated genes: loss or new function? BioEssays 20: 785-788.
72. Wolbang CM, Chandler PM, Smith JJ, Ross JJ. 2004. Auxin from the developing inflorescence is required for the biosynthesis of active gibberellins in barley stems. Plant Physiology 134: 769-776.
73. Wu H, Mori A, Jiang X, Wang Y, Yang M. 2006a. The INDEHISCENT protein regulates unequal cell divisions in Arabidopsis fruit. Planta 224: 971-979.
74. Wu M-F, Tian Q, Reed JW. 2006b. Arabidopsis microRNA167 controls patterns of ARF6 and ARF8 expression, and regulates both female and male reproduction. Development 133: 4211-4218.
75. Yamaguchi S. 2008. Gibberellin metabolism and its regulation. Annual Review of Plant Biology 59: 225-251.