Concerted evolution of D1 and D2 to regulate chlorophyll degradation in soybean

Plant Journal

Volumn 77, Issue 5, 2014, Pages 700-712

  Fang, Chao ^a,b   Li, Congcong ^a,b   Li, Weiyu ^a   Wang, Zheng ^a   Zhou, Zhengkui ^a   Shen, Yanting ^a,b   Wu, Mian ^a   Wu, Yunshuai ^a   Li, Guiquan ^c   Kong, Ling An ^d   Liu, Cuimin ^a   Jackson, Scott A ^e   Tian, Zhixi ^a  

^a INSTITUTE OF GENETICS AND DEVELOPMENTAL BIOLOGY   (China)

^b UNIVERSITY OF CHINESE ACADEMY OF SCIENCES   (China)

^c SHANXI AGRICULTURAL UNIVERSITY   (China)

^d INSTITUTE OF PLANT PROTECTION   (China)

^e UNIVERSITY OF GEORGIA   (United States)

Author keywords

duplicated genes; evolution; Glycine max L. Merr; soybean; stay green

Indexed keywords

DUPLICATED GENES; EVOLUTION; GLYCINE MAX; SOYBEAN; STAY-GREEN;

AMINO ACIDS; CELL DEATH; CLONING; GENE EXPRESSION; TISSUE;

NITROGEN FIXATION;

GLYCINE MAX;

CHLOROPHYLL;

CELL DEATH; GENE DUPLICATION; GENE EXPRESSION REGULATION; GENETICS; LONG TERMINAL REPEAT; METABOLISM; MOLECULAR EVOLUTION; PHENOTYPE; SOYBEAN;

CELL DEATH; CHLOROPHYLL; EVOLUTION, MOLECULAR; GENE DUPLICATION; GENE EXPRESSION REGULATION, PLANT; PHENOTYPE; SOYBEANS; TERMINAL REPEAT SEQUENCES;

EID: 84896726477     PISSN: 09607412     EISSN: 1365313X     Source Type: Journal    
DOI: 10.1111/tpj.12419     Document Type: Article

References (70)

1. Agren, J.A., and, Wright, S.I., (2011) Co-evolution between transposable elements and their hosts: a major factor in genome size evolution? Chromosome Res. 19, 777-786.
2. Armstead, I., Donnison, I., Aubry, S., et al. (2007) Cross-species identification of Mendel's I locus. Science, 315, 73.
3. Bhattacharyya, M.K., Smith, A.M., Ellis, T.H.N., Hedley, C., and, Martin, C., (1990) The wrinkled-seed character of pea described by Mendel is caused by a transposon-like insertion in a gene encoding starch-branching enzyme. Cell, 60, 115-122.
4. 2. Ann. Bot. 75, 143-150.
5. Casneuf, T., De Bodt, S., Raes, J., Maere, S., and, Van de Peer, Y., (2006) Nonrandom divergence of gene expression following gene and genome duplications in the flowering plant Arabidopsis thaliana. Genome Biol. 7, R13.
6. Chan, C., Qi, X.P., Li, M.W., Wong, F.L., and, Lam, H.M., (2012) Recent developments of genomic research in soybean. J. Genet. Genomics 39, 317-324.
7. Chang, Y.F., Imam, J.S., and, Wilkinson, M.E., (2007) The nonsense-mediated decay RNA surveillance pathway. Annu. Rev. Biochem. 76, 51-74.
8. Chao, W.S., Liu, V., Thomson, W.W., Platt, K., and, Walling, L.L., (1995) The impact of chlorophyll-retention mutations, d1d2 and cytG1, during embryogeny in soybean. Plant Physiol. 107, 253-262.
9. 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.
10. Conant, G.C., and, Wolfe, K.H., (2008) Turning a hobby into a job: How duplicated genes find new functions. Nat. Rev. Genet. 9, 938-950.
11. Courtial, B., Feuerbach, F., Eberhard, S., Rohmer, L., Chiapello, H., Camilleri, C., and, Lucas, H., (2001) Tnt1 transposition events are induced by in vitro transformation of Arabidopsis thaliana, and transposed copies integrate into genes. Mol. Genet. Genomics 265, 32-42.
12. Du, J., Tian, Z., Sui, Y., Zhao, M., Song, Q., Cannon, S.B., Cregan, P., and, Ma, J., (2012) Pericentromeric effects shape the patterns of divergence, retention, and expression of duplicated genes in the paleopolyploid soybean. Plant Cell, 24, 24-32.
13. Eckhardt, U., Grimm, B., and, Hortensteiner, S., (2004) Recent advances in chlorophyll biosynthesis and breakdown in higher plants. Plant Mol. Biol. 56, 1-14.
14. Edgar, R.C., (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 32, 1792-1797.
15. Fang, C., Li, W.Y., Li, G.Q., et al. (2013) Cloning of Ln gene through combined approach of map-based cloning and association study in soybean. J. Genet. Genomics 40, 93-96.
16. Feschotte, C., (2008) Transposable elements and the evolution of regulatory networks. Nat. Rev. Genet. 9, 397-405.
17. Flagel, L.E., and, Wendel, J.F., (2009) Gene duplication and evolutionary novelty in plants. New Phytol. 183, 557-564.
18. Guiamet, J.J., and, Luquez, V.M., (2001) Effects of the 'stay green' genotype GGd1d1d2d2 on leaf gas exchange, dry matter accumulation and seed yield in soybean (Glycine max L. Merr.). Ann. Bot. 87, 313-318.
19. Guiamet, J.J., Teeri, J.A., and, Nooden, L.D., (1990) Effects of nuclear and cytoplasmic genes altering chlorophyll loss on gas-exchange during monocarpic senescence in soybean. Plant Cell Physiol. 31, 1123-1130.
20. Guiamet, J.J., Schwartz, E., Pichersky, E., and, Nooden, L.D., (1991) Characterization of cytoplasmic and nuclear mutations affecting chlorophyll and chlorophyll-binding proteins during senescence in soybean. Plant Physiol. 96, 227-231.
21. Guiamet, J.J., Tyystjarvi, E., Tyystjarvi, T., John, I., Kairavuo, M., Pichersky, E., and, Nooden, L.D., (2002) Photoinhibition and loss of photosystem II reaction centre proteins during senescence of soybean leaves. Enhancement of photoinhibition by the 'stay-green' mutation cytG. Physiol. Plant. 115, 468-478.
22. Ha, M., Kim, E.D., and, Chen, Z.J., (2009) Duplicate genes increase expression diversity in closely related species and allopolyploids. Proc. Natl Acad. Sci. USA, 106, 2295-2300.
23. Hadley, H., and, Hymowitz, T., (1973) Speciation and cytogenetics. In: Soybeans: Improvement, Production, and Uses. (, Caldwell, B.E., ed) Madison, WI: American Society of Agronomy, pp. 97-116.
24. Hirochika, H., (2001) Contribution of the Tos17 retrotransposon to rice functional genomics. Curr. Opin. Plant Biol. 4, 118-122.
25. Hirochika, H., Sugimoto, K., Otsuki, Y., Tsugawa, H., and, Kanda, M., (1996) Retrotransposons of rice involved in mutations induced by tissue culture. Proc. Natl Acad. Sci. USA 93, 7783-7788.
26. Hortensteiner, S., (2006) Chlorophyll degradation during senescence. Annu. Rev. Plant Biol. 57, 55-77.
27. Hortensteiner, S., and, Krautler, B., (2011) Chlorophyll breakdown in higher plants. Biochim. Biophys. Acta 1807, 977-988.
28. Innan, H., and, Kondrashov, F., (2010) The evolution of gene duplications: classifying and distinguishing between models. Nat. Rev. Genet. 11, 97-108.
29. Jeong, N., Suh, S.J., Kim, M.H., Lee, S., Moon, J.K., Kim, H.S., and, Jeong, S.C., (2012) Ln is a key regulator of leaflet shape and number of seeds per pod in soybean. Plant Cell, 24, 4807-4818.
30. Jiang, H., Li, M., Liang, N., Yan, H., Wei, Y., Xu, X., Liu, J., Xu, Z., Chen, F., and, Wu, G., (2007) Molecular cloning and function analysis of the stay green gene in rice. Plant J. 52, 197-209.
31. Kawase, M., Fukunaga, K., and, Kato, K., (2005) Diverse origins of waxy foxtail millet crops in East and Southeast Asia mediated by multiple transposable element insertions. Mol. Genet. Genomics 274, 131-140.
32. Kerschen, A., Napoli, C.A., Jorgensen, R.A., and, Muller, A.E., (2004) Effectiveness of RNA interference in transgenic plants. FEBS Lett. 566, 223-228.
33. Kuduvalli, P.N., Rao, J.E., and, Craig, N.L., (2001) Target DNA structure plays a critical role in Tn7 transposition. EMBO J. 20, 924-932.
34. Kumar, A., and, Bennetzen, J.L., (1999) Plant retrotransposons. Annu. Rev. Genet. 33, 479-532.
35. Kusaba, M., Ito, H., Morita, R., et al. (2007) Rice NON-YELLOW COLORING1 is involved in light-harvesting complex II and grana degradation during leaf senescence. Plant Cell, 19, 1362-1375.
36. Levin, H.L., and, Moran, J.V., (2011) Dynamic interactions between transposable elements and their hosts. Nat. Rev. Genet. 12, 615-627.
37. Lim, P.O., Kim, H.J., and, Nam, H.G., (2007) Leaf senescence. Annu. Rev. Plant Biol. 58, 115-136.
38. Lin, J.Y., Stupar, R.M., Hans, C., Hyten, D.L., and, Jackson, S.A., (2010) Structural and functional divergence of a 1-Mb duplicated region in the soybean (Glycine max) genome and comparison to an orthologous region from Phaseolus vulgaris. Plant Cell, 22, 2545-2561.
39. Lisch, D., (2012) How important are transposons for plant evolution? Nat. Rev. Genet. 14, 49-61.
40. Ma, J., Devos, K.M., and, Bennetzen, J.L., (2004) Analyses of LTR-retrotransposon structures reveal recent and rapid genomic DNA loss in rice. Genome Res. 14, 860-869.
41. Miyao, A., Tanaka, K., Murata, K., Sawaki, H., Takeda, S., Abe, K., Shinozuka, Y., Onosato, K., and, Hirochika, H., (2003) Target site specificity of the Tos17 retrotransposon shows a preference for insertion within genes and against insertion in retrotransposon-rich regions of the genome. Plant Cell, 15, 1771-1780.
42. Morita, R., Sato, Y., Masuda, Y., Nishimura, M., and, Kusaba, M., (2009) Defect in non-yellow coloring 3, an alpha/beta hydrolase-fold family protein, causes a stay-green phenotype during leaf senescence in rice. Plant J. 59, 940-952.
43. Ren, G., An, K., Liao, Y., Zhou, X., Cao, Y., Zhao, H., Ge, X., and, Kuai, B., (2007) Identification of a novel chloroplast protein AtNYE1 regulating chlorophyll degradation during leaf senescence in Arabidopsis. Plant Physiol. 144, 1429-1441.
44. Roca, M., James, C., Pruzinska, A., Hortensteiner, S., Thomas, H., and, Ougham, H., (2004) Analysis of the chlorophyll catabolism pathway in leaves of an introgression senescence mutant of Lolium temulentum. Phytochemistry, 65, 1231-1238.
45. Roulin, A., Auer, P.L., Libault, M., Schlueter, J., Farmer, A., May, G., Stacey, G., Doerge, R.W., and, Jackson, S.A., (2013) The fate of duplicated genes in a polyploid plant genome. Plant J. 73, 143-153.
46. Sakuraba, Y.,1, Schelbert, S., Park, S.Y., Han, S.H., Lee, B.D., Andres, C.B., Kessler, F., Hortensteiner, S., and, Paek, N.C., (2012) STAY-GREEN and chlorophyll catabolic enzymes interact at light-harvesting complex II for chlorophyll detoxification during leaf senescence in Arabidopsis. Plant Cell, 24, 507-518.
47. Salentijn, E.M.J., Pereira, A., Angenent, G.C., van der Linden, C.G., Krens, F., Smulders, M.J.M., and, Vosman, B., (2007) Plant translational genomics: from model species to crops. Mol. Breeding 20, 1-13.
48. Sato, Y., Morita, R., Nishimura, M., Yamaguchi, H., and, Kusaba, M., (2007) Mendel's green cotyledon gene encodes a positive regulator of the chlorophyll-degrading pathway. Proc. Natl Acad. Sci. USA 104, 14169-14174.
49. Sato, Y., Morita, R., Katsuma, S., Nishimura, M., Tanaka, A., and, Kusaba, M., (2009) Two short-chain dehydrogenase/reductases, NON-YELLOW COLORING 1 and NYC1-LIKE, are required for chlorophyll b and light-harvesting complex II degradation during senescence in rice. Plant J. 57, 120-131.
50. Schelbert, S., Aubry, S., Burla, B., Agne, B., Kessler, F., Krupinska, K., and, Hortensteiner, S., (2009) Pheophytin pheophorbide hydrolase (pheophytinase) is involved in chlorophyll breakdown during leaf senescence in Arabidopsis. Plant Cell, 21, 767-785.
51. Schenk, N., Schelbert, S., Kanwischer, M., Goldschmidt, E.E., Dormann, P., and, Hortensteiner, S., (2007) The chlorophyllases AtCLH1 and AtCLH2 are not essential for senescence-related chlorophyll breakdown in Arabidopsis thaliana. FEBS Lett. 581, 5517-5525.
52. Schlueter, J.A., Lin, J.Y., Schlueter, S.D., et al. (2007) Gene duplication and paleopolyploidy in soybean and the implications for whole genome sequencing. BMC Genomics, 8, 330.
53. Schmutz, J., Cannon, S.B., Schlueter, J., et al. (2010) Genome sequence of the palaeopolyploid soybean. Nature, 463, 178-183.
54. Severin, A.J., Cannon, S.B., Graham, M.M., Grant, D., and, Shoemaker, R.C., (2011) Changes in twelve homoeologous genomic regions in soybean following three rounds of polyploidy. Plant Cell, 23, 3129-3136.
55. Shoemaker, R.C., Schlueter, J., and, Doyle, J.J., (2006) Paleopolyploidy and gene duplication in soybean and other legumes. Curr. Opin. Plant Biol. 9, 104-109.
56. Tamura, K., Dudley, J., Nei, M., and, Kumar, S., (2007) Mega4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol. Biol. Evol. 24, 1596-1599.
57. Thomas, H., (1987) Sid: a mendelian locus controlling thylakoid membrane disassembly in senescing leaves of Festuca pratensis. Theor. Appl. Genet. 73, 551-555.
58. Thomas, H., and, Howarth, C.J., (2000) Five ways to stay green. J. Exp. Bot. 51, Spec No 329-337.
59. Thomas, H., Morgan, W.G., Thomas, A.M., and, Ougham, H.J., (1999) Expression of the stay-green character introgressed into Lolium temulentum Ceres from a senescence mutant of Festuca pratensis. Theor. Appl. Genet. 99, 92-99.
60. Tian, Z., Rizzon, C., Du, J., Zhu, L., Bennetzen, J.L., Jackson, S.A., Gaut, B.S., and, Ma, J., (2009) Do genetic recombination and gene density shape the pattern of DNA elimination in rice long terminal repeat retrotransposons? Genome Res. 19, 2221-2230.
61. Tian, Z., Wang, X., Lee, R., Li, Y., Specht, J.E., Nelson, R.L., McClean, P.E., Qiu, L., and, Ma, J., (2010) Artificial selection for determinate growth habit in soybean. Proc. Natl Acad. Sci. USA 107, 8563-8568.
62. Tian, Z., Zhao, M., She, M., et al. (2012) Genome-wide characterization of nonreference transposons reveals evolutionary propensities of transposons in soybean. Plant Cell, 24, 4422-4436.
63. Trapnell, C., Pachter, L., and, Salzberg, S.L., (2009) TopHat: discovering splice junctions with RNA-Seq. Bioinformatics, 25, 1105-1111.
64. Trapnell, C., Williams, B.A., Pertea, G., Mortazavi, A., Kwan, G., van Baren, M.J., Salzberg, S.L., Wold, B.J., and, Pachter, L., (2010) Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation. Nat. Biotechnol. 28, 511-515.
65. Trapnell, C., Roberts, A., Goff, L., Pertea, G., Kim, D., Kelley, D.R., Pimentel, H., Salzberg, S.L., Rinn, J.L., and, Pachter, L., et al. (2012) Differential gene and transcript expression analysis of RNA-seq experiments with TopHat and Cufflinks. Nat. Protoc. 7, 562-578.
66. Tsukahara, S., Kobayashi, A., Kawabe, A., Mathieu, O., Miura, A., and, Kakutani, T., (2009) Bursts of retrotransposition reproduced in Arabidopsis. Nature, 461, 423-426.
67. Wang, Y., Wang, X., and, Paterson, A.H., (2012) Genome and gene duplications and gene expression divergence: a view from plants. Ann. N. Y. Acad. Sci. 1256, 1-14.
68. Wicker, T., Sabot, F., Hua-Van, A., et al. (2007) A unified classification system for eukaryotic transposable elements. Nat. Rev. Genet. 8, 973-982.
69. Yamazaki, M., Tsugawa, H., Miyao, A., Yano, M., Wu, J., Yamamoto, S., Matsumoto, T., Sasaki, T., and, Hirochika, H., (2001) The rice retrotransposon Tos17 prefers low-copy-number sequences as integration targets. Mol. Genet. Genomics 265, 336-344.
70. Zhang, L., and, Gaut, B.S., (2003) Does recombination shape the distribution and evolution of tandemly arrayed genes (TAGs) in the Arabidopsis thaliana genome? Genome Res. 13, 2533-2540.