Conservation of fruit dehiscence pathways between Lepidium campestre and Arabidopsis thaliana sheds light on the regulation of INDEHISCENT

Plant Journal

Volumn 76, Issue 4, 2013, Pages 545-556

  Lenser, Teresa ^a   Theißen, Günter ^a  

^a FRIEDRICH SCHILLER UNIVERSITY JENA   (Germany)

Author keywords

Arabidopsis thaliana; dehiscence; fruit development; fruit opening; Lepidium campestre; regulatory network evolution

Indexed keywords

ARABIDOPSIS THALIANA; DEHISCENCE; FRUIT DEVELOPMENT; LEPIDIUM CAMPESTRE; REGULATORY NETWORK;

CONSERVATION; DIGITAL STORAGE; GENE EXPRESSION; MORPHOLOGY; PLANTS (BOTANY);

FRUITS;

ARABIDOPSIS THALIANA; BRASSICACEAE; LEPIDIUM; LEPIDIUM CAMPESTRE;

ALCATRAZ PROTEIN, ARABIDOPSIS; ARABIDOPSIS PROTEIN; BASIC HELIX LOOP HELIX TRANSCRIPTION FACTOR; CYTOKINE; DOC1 PROTEIN, HUMAN; HELIX LOOP HELIX PROTEIN; INDEHISCENT PROTEIN, ARABIDOPSIS;

ARABIDOPSIS; ARABIDOPSIS THALIANA; ARTICLE; DEHISCENCE; FRUIT; FRUIT DEVELOPMENT; FRUIT OPENING; GENE EXPRESSION REGULATION; GENETICS; LEPIDIUM; LEPIDIUM CAMPESTRE; METABOLISM; NUCLEOTIDE SEQUENCE; PHYSIOLOGY; REGULATORY NETWORK EVOLUTION; TRANSGENIC PLANT;

ARABIDOPSIS THALIANA; DEHISCENCE; FRUIT DEVELOPMENT; FRUIT OPENING; LEPIDIUM CAMPESTRE; REGULATORY NETWORK EVOLUTION;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; CONSERVED SEQUENCE; CYTOKINES; FRUIT; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENE EXPRESSION REGULATION, PLANT; HELIX-LOOP-HELIX MOTIFS; LEPIDIUM; PLANTS, GENETICALLY MODIFIED;

EID: 84886773723     PISSN: 09607412     EISSN: 1365313X     Source Type: Journal    
DOI: 10.1111/tpj.12321     Document Type: Article

References (68)

1. Abzhanov, A., Extavour, C.G., Groover, A., Hodges, S.A., Hoekstra, H.E., Kramer, E.M., and, Monteiro, A., (2008) Are we there yet? Tracking the development of new model systems. Trends Genet. 24, 353-360.
2. Al-Shehbaz, I.A., (2001) Brassicaceae (Mustard Family). eLS. Chichester, UK: John Wiley & Sons Ltd. doi: 10.1038/npg.els.0003690.
3. Alvarez, J., and, Smyth, D.R., (1999) CRABS CLAW and SPATULA, two Arabidopsis genes that control carpel development in parallel with AGAMOUS. Development, 126, 2377-2386.
4. Arnaud, N., Girin, T., Sorefan, K., Fuentes, S., Wood, T.A., Lawrenson, T., Sablowski, R., and, Ostergaard, L., (2010) Gibberellins control fruit patterning in Arabidopsis thaliana. Genes Dev. 24, 2127-2132.
5. Avino, M., Kramer, E., Donohue, K., Hammel, A., and, Hall, J., (2012) Understanding the basis of a novel fruit type in Brassicaceae: conservation and deviation in expression patterns of six genes. Evodevo, 3, 20.
6. Bartholmes, C., Nutt, P., and, Theissen, G., (2008) Germline transformation of Shepherd's purse (Capsella bursa-pastoris) by the 'floral dip' method as a tool for evolutionary and developmental biology. Gene, 409, 11-19.
7. Bechtold, N., Jaudeau, B., Jolivet, S., Maba, B., Vezon, D., Voisin, R., and, Pelletier, G., (2000) The maternal chromosome set is the target of the T-DNA in the in planta transformation of Arabidopsis thaliana. Genetics, 155, 1875-1887.
8. Bowman, J.L., (2006) Molecules and morphology: comparative developmental genetics of the Brassicaceae. Plant Syst. Evol. 259, 199-215.
9. Bruce, D.M., Farrent, J.W., Morgan, C.L., and, Child, R.D., (2002) Determining the oilseed rape pod strength needed to reduce seed loss due to pod shatter. Biosyst. Eng. 81, 179-184.
10. Cai, S., and, Lashbrook, C.C., (2008) Stamen abscission zone transcriptome profiling reveals new candidates for abscission control: enhanced retention of floral organs in transgenic plants overexpressing Arabidopsis ZINC FINGER PROTEIN2. Plant Physiol. 146, 1305-1321.
11. Chauvaux, N., Child, R., John, K., Ulvskov, P., Borkhardt, B., Prinsen, E., and, Van Onckelen, H.A., (1997) The role of auxin in cell separation in the dehiscence zone of oilseed rape pods. J. Exp. Bot. 48, 1423-1429.
12. Clough, S.J., and, Bent, A.F., (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J. 16, 735-743.
13. Curtis, I.S., and, Nam, H.G., (2001) Transgenic radish (Raphanus sativus L. longipinnatus Bailey) by floral-dip method-plant development and surfactant are important in optimizing transformation efficiency. Transgenic Res. 10, 363-371.
14. De Block, M., Debrouwer, D., and, Moens, T., (1997) The development of a nuclear male sterility system in wheat. Expression of the barnase gene under the control of tapetum specific promoters. Theor. Appl. Genet. 95, 125-131.
15. De Buck, S., Van Montagu, M., and, Depicker, A., (2001) Transgene silencing of invertedly repeated transgenes is released upon deletion of one of the transgenes involved. Plant Mol. Biol. 46, 433-445.
16. De Buck, S., Windels, P., De Loose, M., and, Depicker, A., (2004) Single-copy T-DNAs integrated at different positions in the Arabidopsis genome display uniform and comparable β-glucuronidase accumulation levels. Cell. Mol. Life Sci. 61, 2632-2645.
17. De Paepe, A., De Buck, S., Hoorelbeke, K., Nolf, J., Peck, I., and, Depicker, A., (2009) High frequency of single-copy T-DNA transformants produced by floral dip in CRE-expressing Arabidopsis plants. Plant J. 59, 517-527.
18. Desfeux, C., Clough, S.J., and, Bent, A.F., (2000) Female reproductive tissues are the primary target of Agrobacterium-mediated transformation by the Arabidopsis floral-dip method. Plant Physiol. 123, 895-904.
19. Dinneny, J.R., and, Yanofsky, M.F., (2005) Drawing lines and borders: how the dehiscent fruit of Arabidopsis is patterned. BioEssays, 27, 42-49.
20. Eriksson, D., (2009) Towards the domestication of Lepidium campestre as an undersown oilseed crop. PhD Thesis. Department of Plant Breeding and Biotechnology, Swedish University of Agricultural Sciences, Alnarp, Sweden.
21. Ferrandiz, C., Liljegren, S.J., and, Yanofsky, M.F., (2000) Negative regulation of the SHATTERPROOF genes by FRUITFULL during Arabidopsis fruit development. Science, 289, 436-438.
22. Gerlach, D., (1984) Botanische Mikrotechnik, eine Einführung, 2. Aufl. Georg Thiema Verlag, Stuttgart, 1977.
23. Girin, T., Stephenson, P., Goldsack, C.M.P., Kempin, S.A., Perez, A., Pires, N., Sparrow, P.A., Wood, T.A., Yanofsky, M.F., and, Ostergaard, L., (2010) Brassicaceae INDEHISCENT genes specify valve margin cell fate and repress replum formation. Plant J. 63, 329-338.
24. Girin, T., Paicu, T., Stephenson, P., et al. (2011) INDEHISCENT and SPATULA interact to specify carpel and valve margin tissue and thus promote seed dispersal in Arabidopsis. Plant Cell, 23, 3641-3653.
25. Groszmann, M., Paicu, T., Alvarez, J.P., Swain, S.M., and, Smyth, D.R., (2011) SPATULA and ALCATRAZ are partially redundant, functionally diverging bHLH genes required for Arabidopsis gynoecium and fruit development. Plant J. 68, 816-829.
26. Gu, Q., Ferrandiz, C., Yanofsky, M.F., and, Martienssen, R., (1998) The FRUITFULL MADS-box gene mediates cell differentiation during Arabidopsis fruit development. Development, 125, 1509-1517.
27. Hall, J.C., Tisdale, T.E., Donohue, K., and, Kramer, E.M., (2006) Developmental basis of an anatomical novelty: heteroarthrocarpy in Cakile lanceolata and Erucaria erucarioides (Brassicaceae). Int. J. Plant Sci. 167, 771-789.
28. Heim, M.A., Jakoby, M., Werber, M., Martin, C., Weisshaar, B., and, Bailey, P.C., (2003) The basic helix-loop-helix transcription factor family in plants: a genome-wide study of protein structure and functional diversity. Mol. Biol. Evol. 20, 735-747.
29. Hoekema, A., Hirsch, P.R., Hooykaas, P.J.J., and, Schilperoort, R.A., (1983) A binary plant vector strategy based on separation of vir- and T-region of the Agrobacterium tumefaciens Ti-plasmid. Nature, 303, 179-180.
30. Ito, T., and, Meyerowitz, E.M., (2000) Overexpression of a gene encoding a cytochrome p450, CYP78A9, induces large and seedless fruit in Arabidopsis. Plant Cell, 12, 1541-1550.
31. Kay, P., Groszmann, M., Ross, J.J., Parish, R.W., and, Swain, S.M., (2013) Modifications of a conserved regulatory network involving INDEHISCENT controls multiple aspects of reproductive tissue development in Arabidopsis. New Phytol. 197, 73-87.
32. Koncz, C., and, Schell, J., (1986) The promoter of TL-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.
33. Lazo, G.R., Stein, P.A., and, Ludwig, R.A., (1991) A DNA transformation-competent Arabidopsis genomic library in Agrobacterium. Nat. Biotechnol. 9, 963-967.
34. Lease, K.A., Wen, J.Q., Li, J., Doke, J.T., Liscum, E., and, Walker, J.C., (2001) A mutant Arabidopsis heterotrimeric G-protein β subunit affects leaf, flower, and fruit development. Plant Cell, 13, 2631-2641.
35. Li, S.J., Liu, Y.J., Zheng, L.Y., et al,. (2012) The plant-specific G protein γ subunit AGG3 influences organ size and shape in Arabidopsis thaliana. New Phytol. 194, 690-703.
36. Liljegren, S.J., Ditta, G.S., Eshed, H.Y., Savidge, B., Bowman, J.L., and, Yanofsky, M.F., (2000) SHATTERPROOF MADS-box genes control seed dispersal in Arabidopsis. Nature, 404, 766-770.
37. Liljegren, S.J., Roeder, A.H.K., Kempin, S.A., Gremski, K., Ostergaard, L., Guimil, S., Reyes, D.K., and, Yanofsky, M.F., (2004) Control of fruit patterning in Arabidopsis by INDEHISCENT. Cell, 116, 843-853.
38. Lu, C.F., and, Kang, J.L., (2008) Generation of transgenic plants of a potential oilseed crop Camelina sativa by Agrobacterium-mediated transformation. Plant Cell Rep. 27, 273-278.
39. Marsch-Martinez, N., Ramos-Cruz, D., Irepan Reyes-Olalde, J., Lozano-Sotomayor, P., Zuniga-Mayo, V.M., and, de Folter, S., (2012) The role of cytokinin during Arabidopsis gynoecia and fruit morphogenesis and patterning. Plant J. 72, 222-234.
40. Martinez-Trujillo, M., Limones-Briones, V., Cabrera-Ponce, J.L., and, Herrera-Estrella, L., (2004) Improving transformation efficiency of Arabidopsis thaliana by modifying the floral dip method. Plant Mol. Biol. Rep. 22, 63-70.
41. Meakin, P.J., and, Roberts, J.A., (1990) Dehiscence of fruit in oilseed rape (Brassica napus L.) 2. The role of cell-wall degrading enzymes and ethylene. J. Exp. Bot. 41, 1003-1011.
42. Morgan, C.L., Bruce, D.M., Child, R., Ladbrooke, Z.L., and, Arthur, A.E., (1998) Genetic variation for pod shatter resistance among lines of oilseed rape developed from synthetic B. napus. Field Crops Res. 58, 153-165.
43. Mühlhausen, A., Lenser, T., Mummenhoff, K., and, Theißen, G., (2013) Evidence that an evolutionary transition from dehiscent to indehiscent fruits in Lepidium (Brassicaceae) was caused by a change in the control of valve margin identity genes. Plant J. 73, 824-835.
44. Mummenhoff, K., Polster, A., Muhlhausen, A., and, Theissen, G., (2009) Lepidium as a model system for studying the evolution of fruit development in Brassicaceae. J. Exp. Bot. 60, 1503-1513.
45. Muskens, M.W.M., Vissers, A.P.A., Mol, J.N.M., and, Kooter, J.M., (2000) Role of inverted DNA repeats in transcriptional and post-transcriptional gene silencing. Plant Mol. Biol. 43, 243-260.
46. Narita, N.N., Moore, S., Horiguchi, G., Kubo, M., Demura, T., Fukuda, H., Goodrich, J., and, Tsukaya, H., (2004) Overexpression of a novel small peptide ROTUNDIFOLIA4 decreases cell proliferation and alters leaf shape in Arabidopsis thaliana. Plant J. 38, 699-713.
47. Ogawa, M., Kay, P., Wilson, S., and, Swain, S.M., (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.
48. Onate-Sanchez, L., and, Vicente-Carbajosa, J., (2008) DNA-free RNA isolation protocols for Arabidopsis thaliana, including seeds and siliques. BMC Res. Notes, 1, 93.
49. Ostergaard, L., Kempin, S.A., Bies, D., Klee, H.J., and, Yanofsky, M.F., (2006) Pod shatter-resistant Brassica fruit produced by ectopic expression of the FRUITFULL gene. Plant Biotechnol. J. 4, 45-51.
50. Payne, T., Johnson, S.D., and, Koltunow, A.M., (2004) KNUCKLES (KNU) encodes a C2H2 zinc-finger protein that regulates development of basal pattern elements of the Arabidopsis gynoecium. Development, 131, 3737-3749.
51. Petersen, M., Sander, L., Child, R., van Onckelen, H., Ulvskov, P., and, Borkhardt, B., (1996) Isolation and characterisation of a pod dehiscence zone-specific polygalacturonase from Brassica napus. Plant Mol. Biol. 31, 517-527.
52. Qing, C.M., Fan, L., Lei, Y., Bouchez, D., Tourneur, C., Yan, L., and, Robaglia, C., (2000) Transformation of Pakchoi (Brassica rapa L. ssp chinensis) by Agrobacterium infiltration. Mol. Breed. 6, 67-72.
53. Rajani, S., and, Sundaresan, V., (2001) The Arabidopsis myc/bHLH gene ALCATRAZ enables cell separation in fruit dehiscence. Curr. Biol. 11, 1914-1922.
54. Roeder, A.H.K., Ferrandiz, C., and, Yanofsky, M.F., (2003) The role of the REPLUMLESS homeodomain protein in patterning the Arabidopsis fruit. Curr. Biol. 13, 1630-1635.
55. Schubert, D., Lechtenberg, B., Forsbach, A., Gils, M., Bahadur, S., and, Schmidt, R., (2004) Silencing in Arabidopsis T-DNA transformants: the predominant role of a gene-specific RNA sensing mechanism versus position effects. Plant Cell, 16, 2561-2572.
56. Smyth, D.R., Bowman, J.L., and, Meyerowitz, E.M., (1990) Early flower development in Arabidopsis. Plant Cell, 2, 755-767.
57. Sorefan, K., Girin, T., Liljegren, S.J., Ljung, K., Robles, P., Galvan-Ampudia, C.S., Offringa, R., Friml, J., Yanofsky, M.F., and, Ostergaard, L., (2009) A regulated auxin minimum is required for seed dispersal in Arabidopsis. Nature, 459, 583-586.
58. Spence, J., Vercher, Y., Gates, P., and, Harris, N., (1996) 'Pod shatter' in Arabidopsis thaliana, Brassica napus and B. juncea. J. Microsc. 181, 195-203.
59. Srivastava, V., Anderson, O.D., and, Ow, D.W., (1999) Single-copy transgenic wheat generated through the resolution of complex integration patterns. Proc. Natl Acad. Sci. USA, 96, 11117-11121.
60. Tague, B.W., (2001) Germ-line transformation of Arabidopsis lasiocarpa. Transgenic Res. 10, 259-267.
61. Toledo-Ortiz, G., Huq, E., and, Quail, P.H., (2003) The Arabidopsis basic/helix-loop-helix transcription factor family. Plant Cell, 15, 1749-1770.
62. Trieu, A.T., Burleigh, S.H., Kardailsky, I.V., et al. (2000) Transformation of Medicago truncatula via infiltration of seedlings or flowering plants with Agrobacterium. Plant J. 22, 531-541.
63. Van Larebeke, N., Engler, G., Holsters, M., Van den Elsacker, S., Zaenen, I., Schilperoort, R.A., and, Schell, J., (1974) Large plasmid in Agrobacterium tumefaciens essential for crown gall-inducing ability. Nature, 252, 169-170.
64. Wang, M.B., and, Waterhouse, P.M., (2000) High-efficiency silencing of a β-glucuronidase gene in rice is correlated with repetitive transgene structure but is independent of DNA methylation. Plant Mol. Biol. 43, 67-82.
65. Wang, W.C., Menon, G., and, Hansen, G., (2003) Development of a novel Agrobacterium-mediated transformation method to recover transgenic Brassica napus plants. Plant Cell Rep. 22, 274-281.
66. Wen, J.Q., Lease, K.A., and, Walker, J.C., (2004) DVL, a novel class of small polypeptides: overexpression alters Arabidopsis development. Plant J. 37, 668-677.
67. Zhang, X.R., Henriques, R., Lin, S.S., Niu, Q.W., and, Chua, N.H., (2006) Agrobacterium-mediated transformation of Arabidopsis thaliana using the floral dip method. Nat. Protoc. 1, 641-646.
68. Zhou, Y., Lu, D.F., Li, C.Y., et al. (2012) Genetic control of seed shattering in rice by the APETALA2 transcription factor SHATTERING ABORTION1. Plant Cell, 24, 1034-1048.