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 Journal

Volumn 73, Issue 5, 2013, Pages 824-835

  Mühlhausen, Andreas ^a   Lenser, Teresa ^b   Mummenhoff, Klaus ^a   Theißen, Günter ^b  

^a UNIVERSITY OF OSNABRÜCK   (Germany)

^b FRIEDRICH SCHILLER UNIVERSITY JENA   (Germany)

Author keywords

Brassicaceae; character evolution; evolutionary developmental biology; fruit dehiscence; L epidium appelianum; L epidium campestre; valve margin

Indexed keywords

BRASSICACEAE; CHARACTER EVOLUTION; DEVELOPMENTAL BIOLOGY; L EPIDIUM APPELIANUM; L EPIDIUM CAMPESTRE; VALVE MARGINS;

GENE EXPRESSION; PLANTS (BOTANY); TISSUE;

FRUITS;

APETALA2 PROTEIN, ARABIDOPSIS; ARABIDOPSIS PROTEIN; HOMEODOMAIN PROTEIN; NUCLEAR PROTEIN; PLANT RNA; VEGETABLE PROTEIN;

ARABIDOPSIS; ARTICLE; BRASSICACEAE; COMPARATIVE STUDY; CYTOLOGY; DNA SEQUENCE; EVOLUTION; FRUIT; GENE EXPRESSION; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; LEPIDIUM; MUTATION; PHENOTYPE; PHYLOGENY; SPECIES DIFFERENCE; TRANSGENIC PLANT; UPREGULATION;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; BIOLOGICAL EVOLUTION; BRASSICACEAE; FRUIT; GENE EXPRESSION; GENE EXPRESSION REGULATION, PLANT; HOMEODOMAIN PROTEINS; LEPIDIUM; MUTATION; NUCLEAR PROTEINS; PHENOTYPE; PHYLOGENY; PLANT PROTEINS; PLANTS, GENETICALLY MODIFIED; RNA, PLANT; SEQUENCE ANALYSIS, DNA; SPECIES SPECIFICITY; UP-REGULATION;

ARABIDOPSIS; ARABIDOPSIS THALIANA; BRASSICACEAE; LEPIDIUM; LEPIDIUM APPELIANUM; LEPIDIUM CAMPESTRE;

EID: 84874501233     PISSN: 09607412     EISSN: 1365313X     Source Type: Journal    
DOI: 10.1111/tpj.12079     Document Type: Article

References (59)

1. Alonso-Cantabrana, H., Ripoll, J.J., Ochando, I., Vera, A., Ferrandiz, C., and, Martinez-Laborda, A., (2007) Common regulatory networks in leaf and fruit patterning revealed by mutations in the Arabidopsis ASYMMETRIC LEAVES1 gene. Development, 134, 2663-2671. (Pubitemid 47225962)
2. Al-Shehbaz, I.A., and, Mummenhoff, K., (2011) Stubendorffia and Winklera belong to the expanded Lepidium (Brassicaceae). Edinb J. Bot. 68, 165-171.
3. Al-Shehbaz, I.A., Mummenhoff, K., and, Appel, O., (2002) Cardaria, Coronopus, and Stroganowia are united with Lepidium (Brassicaceae). Novon, 12, 5-11. (Pubitemid 34527391)
4. Appel, O., and, Al-Shehbaz, I.A., (2003) Cruciferae. In Families and Genera of Vascular Plants, Vol. V (, Kubitzki, K., and, Bayer, C., eds). Berlin/Heidelberg: Springer-Verlag, pp. 75-174.
5. 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.
6. Arnaud, N., Lawrenson, T., Ostergaard, L., and, Sablowski, R., (2011) The same regulatory point mutation changed seed-dispersal structures in evolution and domestication. Curr. Biol. 21, 1-5.
7. Bao, X.Z., Franks, R.G., Levin, J.Z., and, Liu, Z.C., (2004) Repression of AGAMOUS by BELLRINGER in floral and inflorescence meristems. Plant Cell, 16, 1478-1489. (Pubitemid 38774243)
8. 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.
9. Bhatt, A.A., Etchells, J.P., Canales, C., Lagodienko, A., and, Dickinson, H., (2004) VAAMANA-a BEL1-like homeodomain protein, interacts with KNOX proteins BP and STM and regulates inflorescence stem growth in Arabidopsis. Gene, 328, 103-111. (Pubitemid 38352886)
10. Bowman, J.L., Smyth, D.R., and, Meyerowitz, E.M., (1989) Genes directing flower development in Arabidopsis. Plant Cell, 1, 37-52.
11. Byrne, M.E., Groover, A.T., Fontana, J.R., and, Martienssen, R.A., (2003) Phyllotactic pattern and stem cell fate are determined by the Arabidopsis homeobox gene BELLRINGER. Development, 130, 3941-3950. (Pubitemid 37063414)
12. Cai, S.Q., 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. (Pubitemid 352844151)
13. Chen, X.M., (2004) A microRNA as a translational repressor of APETALA2 in Arabidopsis flower development. Science, 303, 2022-2025.
14. Cole, M., Nolte, C., and, Werr, W., (2006) Nuclear import of the transcription factor SHOOT MERISTEMLESS depends on heterodimerization with BLH proteins expressed in discrete sub-domains of the shoot apical meristem of Arabidopsis thaliana. Nucleic Acids Res. 34, 1281-1292.
15. Couvreur, T.L.P., Franzke, A., Al-Shehbaz, I.A., Bakker, F.T., Koch, M.A., and, Mummenhoff, K., (2010) Molecular phylogenetics, temporal diversification, and principles of evolution in the mustard family (Brassicaceae). Mol. Biol. Evol. 27, 55-71.
16. Dinneny, J.R., and, Yanofsky, M.F., (2005) Drawing lines and borders: how the dehiscent fruit of Arabidopsis is patterned. BioEssays, 27, 42-49. (Pubitemid 40128621)
17. Dinneny, J.R., Yadegari, R., Fischer, R.L., Yanofsky, M.F., and, Weigel, D., (2004) The role of JAGGED in shaping lateral organs. Development, 131, 1101-1110. (Pubitemid 38380463)
18. Dinneny, J.R., Weigel, D., and, Yanofsky, M.F., (2005) A genetic framework for fruit patterning in Arabidopsis thaliana. Development, 132, 4687-4696. (Pubitemid 41685279)
19. Favaro, R., Pinyopich, A., Battaglia, R., Kooiker, M., Borghi, L., Ditta, G., Yanofsky, M.F., Kater, M.M., and, Colombo, L., (2003) MADS-box protein complexes control carpel and ovule development in Arabidopsis. Plant Cell, 15, 2603-2611. (Pubitemid 37470661)
20. Ferrandiz, C., Gu, Q., Martienssen, R., and, Yanofsky, M.F., (2000a) Redundant regulation of meristem identity and plant architecture by FRUITFULL, APETALA1 and CAULIFLOWER. Development, 127, 725-734. (Pubitemid 30129019)
21. Ferrandiz, C., Liljegren, S.J., and, Yanofsky, M.F., (2000b) Negative regulation of the SHATTERPROOF genes by FRUITFULL during Arabidopsis fruit development. Science, 289, 436-438. (Pubitemid 30490452)
22. Flanagan, C.A., Hu, Y., and, Ma, H., (1996) Specific expression of the AGL1 MADS-box gene suggests regulatory functions in Arabidopsis gynoecium and ovule development. Plant J. 10, 343-353. (Pubitemid 27114552)
23. Force, A., Lynch, M., Pickett, F.B., Amores, A., Yan, Y.L., and, Postlethwait, J., (1999) Preservation of duplicate genes by complementary, degenerative mutations. Genetics, 151, 1531-1545. (Pubitemid 29177561)
24. Franzke, A., Lysak, M.A., Al-Shehbaz, I.A., Koch, M.A., and, Mummenhoff, K., (2011) Cabbage family affairs: the evolutionary history of Brassicaceae. Trends Plant Sci. 16, 108-116.
25. Frohman, M.A., Dush, M.K., and, Martin, G.R., (1988) Rapid production of full-lenght cDNAs from rare transcripts-amplification using a single gene-specific oligonucleotide primer. Proc. Natl Acad. Sci. USA, 85, 8998-9002. (Pubitemid 19001832)
26. Gasser, C.S., and, Simon, M.K., (2011) Seed dispersal: same gene, different organs. Curr. Biol. 21, R546-R548.
27. 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. (Pubitemid 28239361)
28. Hall, J.C., Sytsma, K.J., and, Iltis, H.H., (2002) Phylogeny of Capparaceae and Brassicaceae based on chloroplast sequence data. Am. J. Bot. 89, 1826-1842. (Pubitemid 35442072)
29. Konishi, S., Izawa, T., Lin, S.Y., Ebana, K., Fukuta, Y., Sasaki, T., and, Yano, M., (2006) An SNP caused loss of seed shattering during rice domestication. Science, 312, 1392-1396. (Pubitemid 43839553)
30. Li, C.B., Zhou, A.L., and, Sang, T., (2006) Rice domestication by reducing shattering. Science, 311, 1936-1939.
31. 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. (Pubitemid 30212404)
32. 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. (Pubitemid 38410729)
33. Ma, H., Yanofsky, M.F., and, Meyerowitz, E.M., (1991) AGL1-AGL6, an Arabidopsis gene family with similarity to floral homeotic and transcription factor genes. Genes Dev. 5, 484-495. (Pubitemid 21905971)
34. 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.
35. Meakin, P.J., and, Roberts, J.A., (1991) Anatomical and biochemical changes associated with the induction of oilseed rape (Brassica napus) pod dehiscence by Dasineura brassicea (Winn.). Ann. Bot. 67, 193-197.
36. Mummenhoff, K., Bruggemann, H., and, Bowman, J.L., (2001) Chloroplast DNA phylogeny and biogeography of Lepidium (Brassicaceae). Am. J. Bot. 88, 2051-2063. (Pubitemid 33649784)
37. Mummenhoff, K., Al-Shehbaz, I.A., Bakker, F.T., Linder, H.P., and, Mühlhausen, A., (2005) Phylogeny, morphological evolution, and speciation of endemic Brassicaceae genera in the Cape flora of southern Africa. Ann. Mo. Bot. Gard. 92, 400-424. (Pubitemid 41546302)
38. 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.
39. Ohno, C.K., Reddy, G.V., Heisler, M.G.B., and, Meyerowitz, E.M., (2004) The Arabidopsis JAGGED gene encodes a zinc finger protein that promotes leaf tissue development. Development, 131, 1111-1122. (Pubitemid 38380464)
40. 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.
41. Pagnussat, G.C., Yu, H.J., Ngo, Q.A., Rajani, S., Mayalagu, S., Johnson, C.S., Capron, A., Xie, L.F., Ye, D., and, Sundaresan, V., (2005) Genetic and molecular identification of genes required for female gametophyte development and function in Arabidopsis. Development, 132, 603-614. (Pubitemid 40277699)
42. Pinyopich, A., Ditta, G.S., Savidge, B., Liljegren, S.J., Baumann, E., Wisman, E., and, Yanofsky, M.F., (2003) Assessing the redundancy of MADS-box genes during carpel and ovule development. Nature, 424, 85-88. (Pubitemid 36834846)
43. Rajani, S., and, Sundaresan, V., (2001) The Arabidopsis myc/bHLH gene ALCATRAZ enables cell separation in fruit dehiscence. Curr. Biol. 11, 1914-1922. (Pubitemid 33146417)
44. Ramakers, C., Ruijter, J.M., Deprez, R.H.L., and, Moorman, A.F.M., (2003) Assumption-free analysis of quantitative real-time polymerase chain reaction (PCR) data. Neurosci. Lett. 339, 62-66. (Pubitemid 36263221)
45. Ripoll, J.J., Roeder, A.H.K., Ditta, G.S., and, Yanofsky, M.F., (2011) A novel role for the floral homeotic gene APETALA2 during Arabidopsis fruit development. Development, 138, 5167-5176.
46. 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. (Pubitemid 37215888)
47. Ruijter, J.M., Ramakers, C., Hoogaars, W.M.H., Karlen, Y., Bakker, O., van den Hoff, M.J.B., and, Moorman, A.F.M., (2009) Amplification efficiency: linking baseline and bias in the analysis of quantitative PCR data. Nucleic Acids Res. 37, e45.
48. Savidge, B., Rounsley, S.D., and, Yanofsky, M.F., (1995) Temporal relationships between the transcription of two Arabidopsis MADS box genes and the floral organ identity genes. Plant Cell, 7, 721-733.
49. Sawa, S., Watanabe, K., Goto, K., Kanaya, E., Morita, E.H., and, Okada, K., (1999) FILAMENTOUS FLOWER, a meristem and organ identity gene of Arabidopsis, encodes a protein with a zinc finger and HMG-related domains. Genes Dev. 13, 1079-1088. (Pubitemid 29233140)
50. Siegfried, K.R., Eshed, Y., Baum, S.F., Otsuga, D., Drews, G.N., and, Bowman, J.L., (1999) Members of the YABBY gene family specify abaxial cell fate in Arabidopsis. Development, 126, 4117-4128. (Pubitemid 29481568)
51. Smith, H.M.S., and, Hake, S., (2003) The interaction of two homeobox genes, BREVIPEDICELLUS and PENNYWISE, regulates internode patterning in the Arabidopsis inflorescence. Plant Cell, 15, 1717-1727. (Pubitemid 37078329)
52. Smyth, D.R., Bowman, J.L., and, Meyerowitz, E.M., (1990) Early flower development in Arabidopsis. Plant Cell, 2, 755-767. (Pubitemid 120015483)
53. 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.
54. 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. (Pubitemid 26098915)
55. Wagner, M., and, Mitchell-Olds, T., (2011) Repeated phenotypic changes highlight molecular targets of convergent evolution. Genome Biol. 12, 124.
56. Warwick, S.I., Mummenhoff, K., Sauder, C.A., Koch, M.A., and, Al-Shehbaz, I.A., (2010) Closing the gaps: phylogenetic relationships in the Brassicaceae based on DNA sequence data of nuclear ribosomal ITS region. Plant Syst. Evol. 285, 209-232.
57. Western, T.L., and, Haughn, G.W., (1999) BELL1 and AGAMOUS genes promote ovule identity in Arabidopsis thaliana. Plant J. 18, 329-336.
58. Wu, H., Mori, A., Jiang, X.S., Wang, Y.X., and, Yang, M., (2006) The INDEHISCENT protein regulates unequal cell divisions in Arabidopsis fruit. Planta, 224, 971-979. (Pubitemid 44286387)
59. Zachgo, S., (2002) In situ hybridization. In Molecular Plant Biology: A Practical Approach, Vol. 2 (, Gillmartin, P., and, Bowler, C., eds). Oxford, UK: IRL Press, pp. 41-63.