Role of B3 domain transcription factors of the AFL family in maize kernel filling

Plant Science

Volumn 236, Issue , 2015, Pages 116-125

  Grimault, Aurélie ^a,b,c,f   Gendrot, Ghislaine ^a,b,c   Chaignon, Sandrine ^a,b,c   Gilard, Françoise ^d   Tcherkez, Guillaume ^d,g   Thévenin, Johanne ^e   Dubreucq, Bertrand ^e   Depège Fargeix, Nathalie ^a,b,c   Rogowsky, Peter M ^a,b,c  

^a UNIVERSITÉ DE LYON   (France)

^b Claud Bernard University Lyon 1   (France)

^c CNRS   (France)

^d INSTITUTE OF PLANT SCIENCES PARIS SACLAY IPS2   (France)

^e INSTITUT JEAN PIERRE BOURGIN   (France)

^f GEOPHYSICAL LABORATORY   (United States)

^g AUSTRALIAN NATIONAL UNIVERSITY   (Australia)

Author keywords

AFL network; Endosperm; Maize; Starch; Transcription factor

Indexed keywords

ARABIDOPSIS THALIANA; BRYOPHYTA; DICOTYLEDONEAE; ZEA MAYS;

PLANT PROTEIN; TRANSCRIPTION FACTOR;

AMINO ACID SEQUENCE; GENE EXPRESSION REGULATION; GENETICS; MAIZE; METABOLISM; MOLECULAR GENETICS; PHYLOGENY; PLANT SEED;

AMINO ACID SEQUENCE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENE EXPRESSION REGULATION, PLANT; MOLECULAR SEQUENCE DATA; PHYLOGENY; PLANT PROTEINS; SEEDS; TRANSCRIPTION FACTORS; ZEA MAYS;

EID: 84927699679     PISSN: 01689452     EISSN: 18732259     Source Type: Journal    
DOI: 10.1016/j.plantsci.2015.03.021     Document Type: Article

References (63)

1. Vernoud V., Hajduch M., Khaled A.-S., Depège N., Rogowsky P.M. Maize embryogenesis. Maydica 2005, 50:469-483.
2. Sreenivasulu N., Wobus U. Seed-development programs: a systems biology-based comparison between dicots and monocots. Annu. Rev. Plant Biol. 2013, 64:189-217.
3. Liu X., Fu J., Gu D., Liu W., Liu T., Peng Y., Wang J., Wang G. Genome-wide analysis of gene expression profiles during the kernel development of maize (Zea mays L.). Genomics 2008, 91:378-387.
4. Sekhon R.S., Hirsch C.N., Childs K.L., Breitzman M.W., Kell P., Duvick S., Spalding E.P., Buell C.R., de Leon N., Kaeppler S.M. Phenotypic and transcriptional analysis of divergently selected maize populations reveals the role of developmental timing in seed size determination. Plant Physiol. 2014, 165:658-669.
5. Lu X., Chen D., Shu D., Zhang Z., Wang W., Klukas C., Chen L.L., Fan Y., Chen M., Zhang C. The differential transcription network between embryo and endosperm in the early developing maize seed. Plant Physiol. 2013, 162:440-455.
6. Li G., Wang D., Yang R., Logan K., Chen H., Zhang S., Skaggs M.I., Lloyd A., Burnett W.J., Laurie J.D., Hunter B.G., Dannenhoffer J.M., Larkins B.A., Drews G.N., Wang X., Yadegari R. Temporal patterns of gene expression in developing maize endosperm identified through transcriptome sequencing. Proc. Natl. Acad. Sci. U. S. A. 2014, 111:7582-7587.
7. Giraudat J., Hauge B.M., Valon C., Smalle J., Parcy F., Goodman H.M. Isolation of the Arabidopsis ABI3 gene by positional cloning. Plant Cell 1992, 4:1251-1261.
8. Luerssen H., Kirik V., Herrmann P., Misera S. FUSCA3 encodes a protein with a conserved VP1/AB13-like B3 domain which is of functional importance for the regulation of seed maturation in Arabidopsis thaliana. Plant J. 1998, 15:755-764.
9. Stone S.L., Kwong L.W., Yee K.M., Pelletier J., Lepiniec L., Fischer R.L., Goldberg R.B., Harada J.J. LEAFY COTYLEDON2 encodes a B3 domain transcription factor that induces embryo development. Proc. Natl. Acad. Sci. U. S. A. 2001, 98:11806-11811.
10. Kwong R.W., Bui A.Q., Lee H., Kwong L.W., Fischer R.L., Goldberg R.B., Harada J.J. LEAFY COTYLEDON1-LIKE defines a class of regulators essential for embryo development. Plant Cell 2003, 15:5-18.
11. Santos Mendoza M., Dubreucq B., Miquel M., Caboche M., Lepiniec L. LEAFY COTYLEDON 2 activation is sufficient to trigger the accumulation of oil and seed specific mRNAs in Arabidopsis leaves. FEBS Lett. 2005, 579:4666-4670.
12. Braybrook S.A., Harada J.J. LECs go crazy in embryo development. Trends Plant Sci. 2008, 13:624-630.
13. Meinke D.W., Franzmann L.H., Nickle T.C., Yeung E.C. Leafy cotyledon mutants of Arabidopsis. Plant Cell 1994, 6:1049-1064.
14. Keith K., Kraml M., Dengler N.G., McCourt P. fusca3: a heterochronic mutation affecting late embryo development in Arabidopsis. Plant Cell 1994, 6:589-600.
15. Nambara E., Keith K., Mccourt P., Naito S. A regulatory role for the Abi3 gene in the establishment of embryo maturation in Arabidopsis thaliana. Development 1995, 121:629-636.
16. Barthole G., To A., Marchive C., Brunaud V., Soubigou-Taconnat L., Berger N., Dubreucq B., Lepiniec L., Baud S. MYB118 represses endosperm maturation in seeds of Arabidopsis. Plant Cell 2014, 26:3519-3537.
17. Kroj T., Savino G., Valon C., Giraudat J., Parcy F. Regulation of storage protein gene expression in Arabidopsis. Development 2003, 130:6065-6073.
18. To A., Valon C., Savino G., Guilleminot J., Devic M., Giraudat J., Parcy F. A network of local and redundant gene regulation governs Arabidopsis seed maturation. Plant Cell 2006, 18:1642-1651.
19. Monke G., Altschmied L., Tewes A., Reidt W., Mock H.P., Baumlein H., Conrad U. Seed-specific transcription factors ABI3 and FUS3: molecular interaction with DNA. Planta 2004, 219:158-166.
20. Wang F., Perry S.E. Identification of direct targets of FUSCA3, a key regulator of Arabidopsis seed development. Plant Physiol. 2013, 161:1251-1264.
21. Kagaya Y., Toyoshima R., Okuda R., Usui H., Yamamoto A., Hattori T. LEAFY COTYLEDON1 controls seed storage protein genes through its regulation of FUSCA3 and ABSCISIC ACID INSENSITIVE3. Plant Cell Physiol. 2005, 46:399-406.
22. Mu J., Tan H., Zheng Q., Fu F., Liang Y., Zhang J., Yang X., Wang T., Chong K., Wang X.J., Zuo J. LEAFY COTYLEDON1 is a key regulator of fatty acid biosynthesis in Arabidopsis. Plant Physiol. 2008, 148:1042-1054.
23. Stone S.L., Braybrook S.A., Paula S.L., Kwong L.W., Meuser J., Pelletier J., Hsieh T.F., Fischer R.L., Goldberg R.B., Harada J.J. Arabidopsis LEAFY COTYLEDON2 induces maturation traits and auxin activity: implications for somatic embryogenesis. Proc. Natl. Acad. Sci. U. S. A. 2008, 105:3151-3156.
24. Baud S., Mendoza M.S., To A., Harscoet E., Lepiniec L., Dubreucq B. WRINKLED1 specifies the regulatory action of LEAFY COTYLEDON2 towards fatty acid metabolism during seed maturation in Arabidopsis. Plant J. 2007, 50:825-838.
25. Che N.Y., Yang Y., Li Y.D., Wang L.L., Huang P., Gao Y., An C.C. Efficient LEC2 activation of OLEOSIN expression requires two neighboring RY elements on its promoter. Sci. China Ser. C 2009, 52:854-863.
26. Braybrook S.A., Stone S.L., Park S., Bui A.Q., Le B.H., Fischer R.L., Goldberg R.B., Harada J.J. Genes directly regulated by LEAFY COTYLEDON2 provide insight into the control of embryo maturation and somatic embryogenesis. Proc. Natl. Acad. Sci. U. S. A. 2006, 103:3468-3473.
27. McCarty D.R., Hattori T., Carson C.B., Vasil V., Lazar M., Vasil I.K. The Viviparous-1 developmental gene of maize encodes a novel transcriptional activator. Cell 1991, 66:895-905.
28. Parcy F., Valon C., Raynal M., Gaubier-Comella P., Delseny M., Giraudat J. Regulation of gene expression programs during Arabidopsis seed development: roles of the ABI3 locus and of endogenous abscisic acid. Plant Cell 1994, 6:1567-1582.
29. Suzuki M., Kao C.Y., McCarty D.R. The conserved B3 domain of VIVIPAROUS1 has a cooperative DNA binding activity. Plant Cell 1997, 9:799-807.
30. Suzuki M., Kao C.Y., Cocciolone S., McCarty D.R. Maize VP1 complements Arabidopsis abi3 and confers a novel ABA/auxin interaction in roots. Plant J. 2001, 28:409-418.
31. Suzuki M., Ketterling M.G., Li Q.B., McCarty D.R. Viviparous1 alters global gene expression patterns through regulation of abscisic acid signaling. Plant Physiol. 2003, 132:1664-1677.
32. Pouvreau B., Baud S., Vernoud V., Morin V., Py C., Gendrot G., Pichon J.P., Rouster J., Paul W., Rogowsky P.M. Duplicate maize Wrinkled1 transcription factors activate target genes involved in seed oil biosynthesis. Plant Physiol. 2011, 156:674-686.
33. Shen B., Allen W.B., Zheng P., Li C., Glassman K., Ranch J., Nubel D., Tarczynski M.C. Expression of ZmLEC1 and ZmWRI1 increases seed oil production in maize. Plant Physiol. 2010, 153:980-987.
34. Barthole G., Lepiniec L., Rogowsky P.M., Baud S. Controlling lipid accumulation in cereal grains. Plant Sci. 2012, 185-186:33-39.
35. Rolletschek H., Koch K., Wobus U., Borisjuk L. Positional cues for the starch/lipid balance in maize kernels and resource partitioning to the embryo. Plant J. 2005, 42:69-83.
36. Wang J.C., Xu H., Zhu Y., Liu Q.Q., Cai X.L. OsbZIP58, a basic leucine zipper transcription factor, regulates starch biosynthesis in rice endosperm. J. Exp. Bot. 2013, 64:3453-3466.
37. Vicente-Carbajosa J., Moose S.P., Parsons R.L., Schmidt R.J. A maize zinc-finger protein binds the prolamin box in zein gene promoters and interacts with the basic leucine zipper transcriptional activator Opaque2. Proc. Natl. Acad. Sci. U. S. A. 1997, 94:7685-7690.
38. Javelle M., Vernoud V., Depege-Fargeix N., Arnould C., Oursel D., Domergue F., Sarda X., Rogowsky P.M. Overexpression of the epidermis-specific homeodomain-leucine zipper IV transcription factor Outer Cell Layer1 in maize identifies target genes involved in lipid metabolism and cuticle biosynthesis. Plant Physiol. 2010, 154:273-286.
39. Xing Q., Creff A., Waters A., Tanaka H., Goodrich J., Ingram G.C. ZHOUPI controls embryonic cuticle formation via a signalling pathway involving the subtilisin protease ABNORMAL LEAF-SHAPE1 and the receptor kinases GASSHO1 and GASSHO2. Development 2013, 140:770-779.
40. Tcherkez G., Mahe A., Gauthier P., Mauve C., Gout E., Bligny R., Cornic G., Hodges M. In folio respiratory fluxomics revealed by 13C isotopic labeling and H/D isotope effects highlight the noncyclic nature of the tricarboxylic acid cycle in illuminated leaves. Plant Physiol. 2009, 151:620-630.
41. Hendriks J.H., Kolbe A., Gibon Y., Stitt M., Geigenberger P. ADP-glucose pyrophosphorylase is activated by posttranslational redox-modification in response to light and to sugars in leaves of Arabidopsis and other plant species. Plant Physiol. 2003, 133:838-849.
42. Thévenin J., Dubos C., Xu W., Le Gourrierec J., Kelemen Z., Charlot F., Nogué F., Lepiniec L., Dubreucq B. A new system for fast and quantitative analysis of heterologous gene expression in plants. New Phytol. 2012, 193:504-512.
43. McCarty D.R., Carson C.B., Stinard P.S., Robertson D.S. Molecular analysis of viviparous-1: an abscisic acid-insensitive mutant of maize. Plant Cell 1989, 1:523-532.
44. Swaminathan K., Peterson K., Jack T. The plant B3 superfamily. Trends Plant Sci. 2008, 13:647-655.
45. Murat F., Xu J.H., Tannier E., Abrouk M., Guilhot N., Pont C., Messing J., Salse J. Ancestral grass karyotype reconstruction unravels new mechanisms of genome shuffling as a source of plant evolution. Genome Res. 2010, 20:1545-1557.
46. Emrich S.J., Li L., Wen T.J., Yandeau-Nelson M.D., Fu Y., Guo L., Chou H.H., Aluru S., Ashlock D.A., Schnable P.S. Nearly identical paralogs: implications for maize (Zea mays L.) genome evolution. Genetics 2007, 175:429-439.
47. Peng F.Y., Weselake R.J. Genome-wide identification and analysis of the B3 superfamily of transcription factors in Brassicaceae and major crop plants. Theor. Appl. Genet. 2013, 126:1305-1319.
48. Marella H.H., Sakata Y., Quatrano R.S. Characterization and functional analysis of ABSCISIC ACID INSENSITIVE3-like genes from Physcomitrella patens. Plant J. 2006, 46:1032-1044.
49. Li Y., Jin K., Zhu Z., Yang J. Stepwise origin and functional diversification of the AFL subfamily B3 genes during land plant evolution. J. Bioinform. Comput. Biol. 2010, 8(Suppl. 1):33-45.
50. Schmid M., Davison T.S., Henz S.R., Pape U.J., Demar M., Vingron M., Scholkopf B., Weigel D., Lohmann J.U. A gene expression map of Arabidopsis thaliana development. Nat. Genet. 2005, 37:501-506.
51. Winter D., Vinegar B., Nahal H., Ammar R., Wilson G.V., Provart N.J. An electronic fluorescent pictograph browser for exploring and analyzing large-scale biological data sets. PLoS ONE 2007, 2:e718.
52. Le B.H., Cheng C., Bui A.Q., Wagmaister J.A., Henry K.F., Pelletier J., Kwong L., Belmonte M., Kirkbride R., Horvath S., Drews G.N., Fischer R.L., Okamuro J.K., Harada J.J., Goldberg R.B. Global analysis of gene activity during Arabidopsis seed development and identification of seed-specific transcription factors. Proc. Natl. Acad. Sci. U. S. A. 2010, 107:8063-8070.
53. Jia H., McCarty D.R., Suzuki M. Distinct roles of LAFL network genes in promoting the embryonic seedling fate in the absence of VAL repression. Plant Physiol. 2013, 163:1293-1305.
54. Sekhon R.S., Lin H., Childs K.L., Hansey C.N., Buell C.R., de Leon N., Kaeppler S.M. Genome-wide atlas of transcription during maize development. Plant J. 2011, 66:553-563.
55. Rikiishi K., Maekawa M. Seed maturation regulators are related to the control of seed dormancy in wheat (Triticum aestivum L.). PLoS ONE 2014, 9:e107618.
56. McKibbin R.S., Wilkinson M.D., Bailey P.C., Flintham J.E., Andrew L.M., Lazzeri P.A., Gale M.D., Lenton J.R., Holdsworth M.J. Transcripts of Vp-1 homeologues are misspliced in modern wheat and ancestral species. Proc. Natl. Acad. Sci. U. S. A. 2002, 99:10203-10208.
57. Cao X., Costa L.M., Biderre-Petit C., Kbhaya B., Dey N., Perez P., McCarty D.R., Gutierrez-Marcos J.F., Becraft P.W. Abscisic acid and stress signals induce Viviparous1 expression in seed and vegetative tissues of maize. Plant Physiol. 2007, 143:720-731.
58. Peng L.T., Shi Z.Y., Li L., Shen G.Z., Zhang J.L. Overexpression of transcription factor OsLFL1 delays flowering time in Oryza sativa. J. Plant Physiol. 2008, 165:876-885.
59. Kobayashi T., Ogo Y., Aung M.S., Nozoye T., Itai R.N., Nakanishi H., Yamakawa T., Nishizawa N.K. The spatial expression and regulation of transcription factors IDEF1 and IDEF2. Ann. Bot. 2010, 105:1109-1117.
60. Prioul J.L., Jeannette E., Reyss A., Gregory N., Giroux M., Hannah L.C., Causse M. Expression of ADP-glucose pyrophosphorylase in maize (Zea mays L.) grain and source leaf during grain filling. Plant Physiol. 1994, 104:179-187.
61. Charlton W.L., Keen C.L., Merriman C., Lynch P., Greenland A.J., Dickinson H.G. Endosperm development in Zea mays - implication of gametic imprinting and paternal excess in regulation of transfer layer development. Development 1995, 121:3089-3097.
62. Gibbon B.C., Larkins B.A. Molecular genetic approaches to developing quality protein maize. Trends Genet. 2005, 21:227-233.
63. Lotan T., Ohto M., Yee K.M., West M.A.L., Lo R., Kwong R.W., Yamagishi K., Fischer R.L., Goldberg R.B., Harada J.J. Arabidopsis LEAFY COTYLEDON1 is sufficient to induce embryo development in vegetative cells. Cell 1998, 93:1195-1205.