Understanding the basis of a novel fruit type in Brassicaceae: conservation and deviation in expression patterns of six genes

EvoDevo

Jocelyn C Hall²  Alexander J Hammel²  Kathleen Donohue³  Elena M Kramer¹  Mariano Avino² 

[1] Department of Organismal and Evolutionary Biology, Harvard University, Cambridge, MA, 02138, USA;Department of Biological Sciences, University of Alberta, Edmonton, AB, T6G 2E9, CANADA;Department of Biology, Duke University, Durham, NC, 27708, USA

关键词: Silique;    SHATTERPROOF;    REPLUMLESS;    FRUITFULL;    INDEHISCENT;    Fruit development;    Brassicaceae;    ALCATRAZ;   

Others  :  807505
DOI  :  10.1186/2041-9139-3-20

 received in 2012-03-16, accepted in 2012-06-28,  发布年份 2012

【 摘 要 】

Background

Variation in fruit morphology is important for plant fitness because it influences dispersal capabilities. Approximately half the members of tribe Brassiceae (Brassicaceae) exhibit fruits with segmentation and variable dehiscence, called heteroarthrocarpy. The knowledge of the genetics of fruit patterning in Arabidopsis offers the opportunity to ask: (1) whether this genetic pathway is conserved in taxa with different fruit morphologies; (2) how the pathway may be modified to produce indehiscence; and (3) whether the pathway has been recruited for a novel abscission zone.

Methods

We identified homologs of ALCATRAZ, FRUITFULL, INDEHISCENT, SHATTERPROOF, and REPLUMLESS from two taxa, representing different types of heteroarthrocarpy. Comparative gene expression of twelve loci was assessed to address how their expression may have been modified to produce heteroarthrocarpy.

Results

Studies demonstrated overall conservation in gene expression patterns between dehiscent segments of Erucaria erucarioides and Arabidopsis, with some difference in expression of genes that position the valve margin. In contrast, indehiscence in heteroarthrocarpic fruit segments was correlated with the elimination of the entire valve margin pathway in Erucaria and Cakile lanceolata as well as its absence from a novel lateral abscission zone.

Conclusions

These findings suggest that modifications in the valve margin positioning genes are responsible for differences between heteroarthrocarpic and Arabidopsis-like fruits and support the hypothesis that heteroarthrocarpy evolved via repositioning the valve margin. They also highlight conservation in the dehiscence pathway across Brassicaceae.

【 授权许可】

   
2012 Avino et al.; licensee BioMed Central Ltd.

【 图 表 】

Figure 1.

Figure 2.

Figure 3.

Figure 4.

Figure 5.

【 参考文献 】

• [1]Hall JC, Donohue K: Genetics of Plant Dispersal. In Dispersal: causes and consequences. Edited by Clobert J, Baguette M, Benton T, Bullock J. New York, NY: Oxford University Press; in press
• [2]Bolmgren K, Eriksson O: Fleshy fruits - origins, niche shifts, and diversification. Oikos 2005, 109:255-272.
• [3]Lorts CM, Briggeman T, Sang T: Evolution of fruit types and seed dispersal: A phylogenetic and ecological snapshot. J Syst Evol 2008, 46:396-404.
• [4]Knapp S: Tobacco to tomatoes: a phylogenetic perspective on fruit diversity in the Solanaceae. J Exp Bot 2002, 53:2001-2022.
• [5]Clausing G, Meyer K, Renner SS: Correlations among fruit traits and evolution of different fruits within Melastomataceae. Bot J Linn Soc 2000, 133:303-326.
• [6]Appel O, Al-Shehbaz IA: Cruciferae. In The Families and Genera of Vascular Plants. Volume V. Flowering plants, Dicotyledons: Malvales, Capparales, and Non-betalain Caryophyllales. Edited by Kubitzki K, Bayer C. Berlin: Springer; 2003:75-174.
• [7]Koch M, Al-Shehbaz IA, Mummenhoff K: Molecular systematics, evolution, and population biology in the mustard family (Brassicaceae). Ann Mo Bot Gard 2003, 90:151-171.
• [8]Mummenhoff K, Polster A, Muhlhausen A, Theissen G: Lepidium as a model system for studying the evolution of fruit development in Brassicaceae. J Exp Bot 2009, 60:1503-1513.
• [9]Doyle J, Luckow M: The rest of the iceberg. Legume diversity and evolution in a phylogenetic context. Plant Physiol 2003, 131:900-910.
• [10]Lewis MW, Leslie ME, Liljegren SJ: Plant separation: 50 ways to leave your mother. Curr Opin Plant Biol 2006, 9:59-65.
• [11]Dinneny JR, Weigel D, Yanofsky MF: A genetic framework for fruit patterning in Arabidopsis thaliana. Development 2005, 132:4687-4696.
• [12]Dinneny JR, Yanofsky MF: Drawing line and borders: how the dehiscent fruit of Arabidopsis is patterned. Bioessays 2004, 27:42-49.
• [13]Spence J, Vercher Y, Gates P, Harris N: ‘Pod shatter’ in Arabidopsis thaliana Brassica napusandB. juncea. J Microsc-Oxf 1996, 181:195-203.
• [14]Liljegren SJ, Roeder AHK, Kempin SA, Gremski K, Østergaard L, Guimil S, Reyes DK, Yanofsky MF: Control of fruit patterning in Arabidopsis by INDEHISCENT. Cell 2004, 116:843-853.
• [15]Flanagan CA, Hu Y, Ma H: Specific expression of the AGL1 MADS-box gene suggests regulatory functions in Arabidopsis gynoecium and ovule development. Plant J 1996, 10:343-353.
• [16]Savidge B, Rounsley SD, Yanofsky MF: Temporal relationship between the transcription of two Arabidopsis MADS box genes and the floral organ identity genes. Plant Cell 1995, 7:721-733.
• [17]Liljegren SJ, Ditta GS, Eshed Y, Savidge B, Bowman JL, Yanofsky MF: SHATTERPROOF MADS-box genes control seed dispersal in Arabidopsis. Nature 2000, 404:766-770.
• [18]Rajani S, Sundaresan V: The Arabidopsis myc/bHLH gene ALCATRAZ enables cell separation in fruit dehiscence. Curr Biol 2001, 11:1914-1922.
• [19]Ferrandiz C, Liljegren SJ, Yanofsky MF: Negative regulation of the SHATTERPROOF genes by FRUITFULL during Arabidopsis fruit development. Science 2000, 289:436-438.
• [20]Roeder AHK, Ferrandiz C, Yanofsky MF: The role of the REPLUMLESS homeodomain protein in patterning of Arabidopsis fruit. Curr Biol 2003, 13:1630-1635.
• [21]Alonso-Cantabrana H, Ripoll JJ, Ochando I, Vera A, Ferrandiz C, Martinez-Laborda A: Common regulatory networks in leaf and fruit patterning revealed by mutations in the Arabidopsis ASYMMETRIC LEAVES1 gene. Development 2007, 134:2663-2671.
• [22]Ripoll JJ, Roeder AHK, Ditta GS, Yanofsky MF: A novel role for the floral homeotic gene APETALA2 during Arabidopsis fruit development. Development 2011, 138:5167-5176.
• [23]Arnaud N, Lawrenson T, Ostergaard L, Sablowski R: The same regulatory point mutation changed seed-dispersal structures in evolution and domestication. Curr Biol 2011, 21:1215-1219.
• [24]Girin T, Stephenson P, Goldsack CMP, Kempin SA, Perez A, Pires N, Sparrow PA, Wood TA, Yanofsky MF, Østergaard L: Brassicaceae INDEHISCENT genes specify valve margin cell fate and repress replum formation. Plant J 2010, 63:329-338.
• [25]Ostergaard L, Kempin SA, Bies D, Klee HJ, Yanofsky MF: Pod shatter-resistant Brassica fruit produced by ectopic expression of the FRUITFULL gene. Plant Biotechnol J 2006, 4:45-51.
• [26]Bailey CD, Koch MA, Mayer M, Mummenhoff K, O’Kane SL, Warwick SI, Windham MD, Al-Shehbaz IA: Toward a global phylogeny of the Brassicaceae. Mol Biol Evol 2006, 23:2142-2160.
• [27]Warwick SI, Sauder CA: Phylogeny of tribe Brassiceae (Brassicaceae) based on chloroplast restriction site polymorphisms and nuclear ribosomal internal transcribed spacer and chloroplast trnL intron sequences. Can Journal Bot-Rev CanDe Botanique 2005, 83:467-483.
• [28]Hall JC, Tisdale TE, Donohue K, Wheeler A, Al-Yahya MA, Kramer EM: Convergent evolution of a complex fruit structure in the tribe Brassiceae (Brassicaceae). Am J Bot 2011, 98:1989-2003.
• [29]Hall JC, Tisdale TE, Donohue K, Kramer EM: Developmental basis of an anatomical novelty: heteroarthrocarpy in Cakile lanceolata and Erucaria erucarioides (Brassicaceae). Int J Plant Sci 2006, 167:771-789.
• [30]Appel O: The so-called ‘beak’, a character in the systematics of Brassicaceae? Bot Jahrb Syst Pflanzengesch Pflanzengeogr 1999, 121:85-98.
• [31]Zohary M: Carpological stuides in Cruciferae. Palest J Bot, Jerusalem Series 1948, 4:158-165.
• [32]Imbert E: Ecological consequences and ontogeny of seed heteromorphism. Perspect Plant Ecol Evol Syst 2002, 5:13-36.
• [33]Rodman JE: Systematics and evolution of the genus Cakile (Cruciferae). Contrib from the Gray Herbarium 1974, 205:3-146.
• [34]Donohue K: Maternal determinants of seed dispersal in Cakile edentula: Fruit, plant, and site traits. Ecology 1998, 79:2771-2788.
• [35]Taghizadeh MS, Crawford S, Nicolas ME, Cousens RD: Water deficit changes the anatomy of the fruit abscission zone in Raphanus raphanistrum (Brassicaceae). Aust J Bot 2009, 57:708-714.
• [36]Kramer EM, Dorit RL, Irish VF: Molecular evolution of genes controlling petal and stamen development: Duplication and divergence within the APETALA3 and PISTILLATA MADS-box gene lineages. Genetics 1998, 149:765-783.
• [37]Hall AE: BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucl Acids Symp Ser 1999, 41:95-98.
• [38]Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S: MEGA5: Molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 2011, 28:2731-2739.
• [39]Kramer EM: Methods for studying the evolution of plant reproductive structures: Comparative gene expression techniques. In Molecular Evolution: Producing the Biochemical Data, Part B. Methods in Enzymology, volume 395. Edited by Zimmer EA, Waltham RE. MA: Academic; 2005:617-636.
• [40]Jackson D: In situhybridisation in plants. In Molecular plant pathology, a practical approach. Edited by Bowles DJ, Gurr SJ, McPherson P. Oxford: Oxford University Press; 1991.
• [41]Lysak MA, Koch MA, Pecinka A, Schubert I: Chromosome triplication found across the tribe Brassiceae. Genome Res 2005, 15:516-525.
• [42]Parkin IAP, Gulden SM, Sharpe AG, Lukens L, Trick M, Osborn TC, Lydiate DJ: Segmental structure of the Brassica napus genome based on comparative analysis with Arabidopsis thaliana. Genetics 2005, 171:765-781.
• [43]Kramer EM, Jaramillo MA, Di Stilio VS: Patterns of gene duplication and functional evolution during the diversification of the AGAMOUS subfamily of MADS box genes in angiosperms. Genetics 2004, 166:1011-1023.
• [44]Zahn LM, Leebens-Mack JH, Arrington JM, Hu Y, Landherr LL, dePamphilis CW, Becker A, Theissen G, Ma H: Conservation and divergence in the AGAMOUS subfamily of MADS-box genes: evidence of independent sub- and neofunctionalization events. Evol Dev 2006, 8:30-45.
• [45]Tan XL, Xia ZW, Zhang LL, Zhang ZY, Guo ZJ, Qi CK: Cloning and sequence analysis of oilseed rape (Brassica napus) SHP2 gene. Bot Stud 2009, 50:403-412.
• [46]Mandel MA, Yanofsky MF: The Arabidopsis AGL8 MADS-Box gene is expressed in inflorescence meristems and is negatively regulated by APETALA1. Plant Cell 1995, 7:1763-1771.
• [47]Sorefan K, Girin T, Liljegren SJ, Ljung K, Robles P, Galvan-Ampudia CS, Offringa R, Friml J, Yanofsky MF, Østergaard L: A regulated auxin minimum is required for seed dispersal in Arabidopsis. Nature 2009, 459:583-586.
• [48]Gu Q, Ferrandiz C, Yanofsky MF, Martienssen R: The FRUITFULL MADS-box gene mediates cell differentiation during Arabidopsis fruit development. Development 1998, 125:1509-1517.
• [49]Force A, Lynch M, Pickett FB, Amores A, Yan YL, Postlethwait J: Preservation of duplicate genes by complementary, degenerative mutations. Genetics 1999, 151:1531-1545.
• [50]Smith HMS, Hake S: The interaction of two homeobox genes, BREVIPEDICELLUS and PENNYWISE, regulates internode patterning in the Arabidopsis inflorescence. Plant Cell 2003, 15:1717-1727.
• [51]Byrne ME, Groover AT, Fontana JR, Martienssen RA: Phyllotactic pattern and stem cell fate are determined by the Arabidopsis homeobox gene BELLRINGER. Development 2003, 130:3941-3950.
• [52]Pinyopich A, Ditta GS, Savidge B, Liljegren SJ, Baumann E, Wisman E, Yanofsky MF: Assessing the redundancy of MADS-box genes during carpel and ovule development. Nature 2003, 424:85-88.