Ribosomal protein RPL27a promotes female gametophyte development in a dose-dependent manner

Plant Physiology

Volumn 165, Issue 3, 2014, Pages 1133-1143

  Zsögön, Agustin ^a,b   Szakonyi, Dóra ^a,c   Shi, Xiuling ^a   Byrne, Mary E ^a  

^a UNIVERSITY OF SYDNEY   (Australia)

^b UNIVERSITY OF SÃO PAULO   (Brazil)

^c GHENT UNIVERSITY   (Belgium)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 84903650274     PISSN: 00320889     EISSN: 15322548     Source Type: Journal    
DOI: 10.1104/pp.114.241778     Document Type: Article

References (70)

1. Adamski NM, Anastasiou E, Eriksson S, O'Neill CM, Lenhard M (2009) Local maternal control of seed size by KLUH/CYP78A5-dependent growth signaling. Proc Natl Acad Sci USA 106: 20115-20120
2. Alonso JM, Stepanova AN, Leisse TJ, Kim CJ, Chen H, Shinn P, Stevenson DK, Zimmerman J, Barajas P, Cheuk R, et al (2003) Genome-wide insertional mutagenesis of Arabidopsis thaliana. Science 301: 653-657
3. Amsterdam A, Sadler KC, Lai K, Farrington S, Bronson RT, Lees JA, Hopkins N (2004) Many ribosomal protein genes are cancer genes in zebrafish. PLoS Biol 2: E139
4. Barakat A, Szick-Miranda K, Chang IF, Guyot R, Blanc G, Cooke R, Delseny M, Bailey-Serres J (2001) The organization of cytoplasmic ribosomal protein genes in the Arabidopsis genome. Plant Physiol 127: 398-415
5. Bencivenga S, Colombo L, Masiero S (2011) Cross talk between the sporophyte and the megagametophyte during ovule development. Sex Plant Reprod 24: 113-121
6. Bhavsar RB, Makley LN, Tsonis PA (2010) The other lives of ribosomal proteins. Hum Genomics 4: 327-344
7. Bolze A, Mahlaoui N, Byun M, Turner B, Trede N, Ellis SR, Abhyankar A, Itan Y, Patin E, Brebner S, et al (2013) Ribosomal protein SA haploinsufficiency in humans with isolated congenital asplenia. Science 340: 976-978
8. Byrne ME (2009) A role for the ribosome in development. Trends Plant Sci 14: 512-519
9. Byrne ME, Simorowski J, Martienssen RA (2002) ASYMMETRIC LEAVES1 reveals knox gene redundancy in Arabidopsis. Development 129: 1957-1965
10. Carroll AJ, Heazlewood JL, Ito J, Millar AH (2008) Analysis of the Arabidopsis cytosolic ribosome proteome provides detailed insights into its components and their post-translational modification. Mol Cell Proteomics 7: 347-369
11. Casanova-Sáez R, Candela H, Micol JL (2014) Combined haploinsufficiency and purifying selection drive retention of RPL36a paralogs in Arabidopsis. Sci Rep 4: 4122
12. Chantha SC, Gray-Mitsumune M, Houde J, Matton DP (2010) The MIDASIN and NOTCHLESS genes are essential for female gametophyte development in Arabidopsis thaliana. Physiol Mol Biol Plants 16: 3-18
13. Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16: 735-743
14. Creff A, Sormani R, Desnos T (2010) The two Arabidopsis RPS6 genes, encoding for cytoplasmic ribosomal proteins S6, are functionally equivalent. Plant Mol Biol 73: 533-546
15. Curtis MD, Grossniklaus U (2003) A gateway cloning vector set for highthroughput functional analysis of genes in planta. Plant Physiol 133: 462-469
16. Draptchinskaia N, Gustavsson P, Andersson B, Pettersson M, Willig TN, Dianzani I, Ball S, Tchernia G, Klar J, Matsson H, et al (1999) The gene encoding ribosomal protein S19 is mutated in Diamond-Blackfan anaemia. Nat Genet 21: 169-175
17. Falcone Ferreyra ML, Casadevall R, Luciani MD, Pezza A, Casati P (2013) New evidence for differential roles of L10 ribosomal proteins from Arabidopsis. Plant Physiol 163: 378-391
18. Falcone Ferreyra ML, Pezza A, Biarc J, Burlingame AL, Casati P (2010) Plant L10 ribosomal proteins have different roles during development and translation under ultraviolet-B stress. Plant Physiol 153: 1878-1894
19. Farrar JE, Nater M, Caywood E, McDevitt MA, Kowalski J, Takemoto CM, Talbot CC Jr, Meltzer P, Esposito D, Beggs AH, et al (2008) Abnormalities of the large ribosomal subunit protein, Rpl35a, in Diamond-Blackfan anemia. Blood 112: 1582-1592
20. Fujikura U, Horiguchi G, Ponce MR, Micol JL, Tsukaya H (2009) Coordination of cell proliferation and cell expansion mediated by ribosomerelated processes in the leaves of Arabidopsis thaliana. Plant J 59: 499-508
21. Gazda HT, Grabowska A, Merida-Long LB, Latawiec E, Schneider HE, Lipton JM, Vlachos A, Atsidaftos E, Ball SE, Orfali KA, et al (2006) Ribosomal protein S24 gene is mutated in Diamond-Blackfan anemia. Am J Hum Genet 79: 1110-1118
22. Gazda HT, Sheen MR, Vlachos A, Choesmel V, O'Donohue MF, Schneider H, Darras N, Hasman C, Sieff CA, Newburger PE, et al (2008) Ribosomal protein L5 and L11 mutations are associated with cleft palate and abnormal thumbs in Diamond-Blackfan anemia patients. Am J Hum Genet 83: 769-780
23. Giavalisco P, Wilson D, Kreitler T, Lehrach H, Klose J, Gobom J, Fucini P (2005) High heterogeneity within the ribosomal proteins of the Arabidopsis thaliana 80S ribosome. Plant Mol Biol 57: 577-591
24. Gilbert WV (2011) Functional specialization of ribosomes? Trends Biochem Sci 36: 127-132
25. Groß-Hardt R, Kägi C, Baumann N, Moore JM, Baskar R, Gagliano WB, Jürgens G, Grossniklaus U (2007) LACHESIS restricts gametic cell fate in the female gametophyte of Arabidopsis. PLoS Biol 5: e47
26. Harscoët E, Dubreucq B, Palauqui JC, Lepiniec L (2010) NOF1 encodes an Arabidopsis protein involved in the control of rRNA expression. PLoS ONE 5: e12829
27. Horiguchi G, Mollá-Morales A, Pérez-Pérez JM, Kojima K, Robles P, Ponce MR, Micol JL, Tsukaya H (2011) Differential contributions of ribosomal protein genes to Arabidopsis thaliana leaf development. Plant J 65: 724-736
28. Horiguchi G, Van Lijsebettens M, Candela H, Micol JL, Tsukaya H (2012) Ribosomes and translation in plant developmental control. Plant Sci 191-192: 24-34
29. Huanca-Mamani W, Garcia-Aguilar M, León-Martínez G, Grossniklaus U, Vielle-Calzada JP (2005) CHR11, a chromatin-remodeling factor essential for nuclear proliferation during female gametogenesis in Arabidopsis thaliana. Proc Natl Acad Sci USA 102: 17231-17236
30. Huang CK, Huang LF, Huang JJ, Wu SJ, Yeh CH, Lu CA (2010) A DEADbox protein, AtRH36, is essential for female gametophyte development and is involved in rRNA biogenesis in Arabidopsis. Plant Cell Physiol 51: 694-706
31. Imai A, Komura M, Kawano E, Kuwashiro Y, Takahashi T (2008) A semidominant mutation in the ribosomal protein L10 gene suppresses the dwarf phenotype of the acl5 mutant in Arabidopsis thaliana. Plant J 56: 881-890
32. Ito T, Kim GT, Shinozaki K (2000) Disruption of an Arabidopsis cytoplasmic ribosomal protein S13-homologous gene by transposon-mediated mutagenesis causes aberrant growth and development. Plant J 22: 257-264
33. Kleinboelting N, Huep G, Kloetgen A, Viehoever P, Weisshaar B (2012) GABI-Kat SimpleSearch: new features of the Arabidopsis thaliana T-DNA mutant database. Nucleic Acids Res 40: D1211-D1215
34. Kondrashov N, Pusic A, Stumpf CR, Shimizu K, Hsieh AC, Xue S, Ishijima J, Shiroishi T, Barna M (2011) Ribosome-mediated specificity in Hox mRNA translation and vertebrate tissue patterning. Cell 145: 383-397
35. Lambertsson A (1998) The minute genes in Drosophila and their molecular functions. Adv Genet 38: 69-134
36. Laubinger S, Zeller G, Henz SR, Sachsenberg T, Widmer CK, Naouar N, Vuylsteke M, Schölkopf B, Rätsch G, Weigel D (2008) At-TAX: a whole genome tiling array resource for developmental expression analysis and transcript identification in Arabidopsis thaliana. Genome Biol 9: R112
37. Li HJ, Liu NY, Shi DQ, Liu J, Yang WC (2010) YAO is a nucleolar WD40-repeat protein critical for embryogenesis and gametogenesis in Arabidopsis. BMC Plant Biol 10: 169
38. Li N, Yuan L, Liu N, Shi D, Li X, Tang Z, Liu J, Sundaresan V, Yang WC (2009) SLOW WALKER2, a NOC1/MAK21 homologue, is essential for coordinated cell cycle progression during female gametophyte development in Arabidopsis. Plant Physiol 151: 1486-1497
39. Liu M, Shi DQ, Yuan L, Liu J, Yang WC (2010) SLOW WALKER3, encoding a putative DEAD-box RNA helicase, is essential for female gametogenesis in Arabidopsis. J Integr Plant Biol 52: 817-828
40. Marygold SJ, Roote J, Reuter G, Lambertsson A, Ashburner M, Millburn GH, Harrison PM, Yu Z, Kenmochi N, Kaufman TC, et al (2007) The ribosomal protein genes and Minute loci of Drosophila melanogaster. Genome Biol 8: R216
41. McCann KL, Baserga SJ (2013) Genetics. Mysterious ribosomopathies. Science 341: 849-850
42. McGowan KA, Li JZ, Park CY, Beaudry V, Tabor HK, Sabnis AJ, Zhang W, Fuchs H, de Angelis MH, Myers RM, et al (2008) Ribosomal mutations cause p53-mediated dark skin and pleiotropic effects. Nat Genet 40: 963-970
43. Missbach S, Weis BL, Martin R, Simm S, Bohnsack MT, Schleiff E (2013) 40S ribosome biogenesis co-factors are essential for gametophyte and embryo development. PLoS ONE 8: e54084
44. Nishimura T, Wada T, Yamamoto KT, Okada K (2005) The Arabidopsis STV1 protein, responsible for translation reinitiation, is required for auxin-mediated gynoecium patterning. Plant Cell 17: 2940-2953
45. Oliver ER, Saunders TL, Tarlé SA, Glaser T (2004) Ribosomal protein L24 defect in belly spot and tail (Bst), a mouse Minute. Development 131: 3907-3920
46. Olmedo-Monfil V, Durán-Figueroa N, Arteaga-Vázquez M, Demesa-Arévalo E, Autran D, Grimanelli D, Slotkin RK, Martienssen RA, Vielle-Calzada JP (2010) Control of female gamete formation by a small RNA pathway in Arabidopsis. Nature 464: 628-632
47. Pinon V, Etchells JP, Rossignol P, Collier SA, Arroyo JM, Martienssen RA, Byrne ME (2008) Three PIGGYBACK genes that specifically influence leaf patterning encode ribosomal proteins. Development 135: 1315-1324
48. Rhee SY, Beavis W, Berardini TZ, Chen G, Dixon D, Doyle A, Garcia-Hernandez M, Huala E, Lander G, Montoya M, et al (2003) The Arabidopsis Information Resource (TAIR): a model organism database providing a centralized, curated gateway to Arabidopsis biology, research materials and community. Nucleic Acids Res 31: 224-228
49. Rosado A, Li R, van de Ven W, Hsu E, Raikhel NV (2012) Arabidopsis ribosomal proteins control developmental programs through translational regulation of auxin response factors. Proc Natl Acad Sci USA 109: 19537-19544
50. Rosado A, Sohn EJ, Drakakaki G, Pan S, Swidergal A, Xiong Y, Kang BH, Bressan RA, Raikhel NV (2010) Auxin-mediated ribosomal biogenesis regulates vacuolar trafficking in Arabidopsis. Plant Cell 22: 143-158
51. Scholl RL, May ST, Ware DH (2000) Seed and molecular resources for Arabidopsis. Plant Physiol 124: 1477-1480
52. Sessions A, Burke E, Presting G, Aux G, McElver J, Patton D, Dietrich B, Ho P, Bacwaden J, Ko C, et al (2002) A high-throughput Arabidopsis reverse genetics system. Plant Cell 14: 2985-2994
53. Shi DQ, Liu J, Xiang YH, Ye D, Sundaresan V, Yang WC (2005) SLOW WALKER1, essential for gametogenesis in Arabidopsis, encodes a WD40 protein involved in 18S ribosomal RNA biogenesis. Plant Cell 17: 2340-2354
54. Stirnberg P, Liu JP, Ward S, Kendall SL, Leyser O (2012) Mutation of the cytosolic ribosomal protein-encoding RPS10B gene affects shoot meristematic function in Arabidopsis. BMC Plant Biol 12: 160
55. Sundaresan V, Springer P, Volpe T, Haward S, Jones JDG, Dean C, Ma H, Martienssen R (1995) Patterns of gene action in plant development revealed by enhancer trap and gene trap transposable elements. Genes Dev 9: 1797-1810
56. Szakonyi D, Byrne ME (2011a) Involvement of ribosomal protein RPL27a in meristem activity and organ development. Plant Signal Behav 6: 712-714
57. Szakonyi D, Byrne ME (2011b) Ribosomal protein L27a is required for growth and patterning in Arabidopsis thaliana. Plant J 65: 269-281
58. Terzian T, Box N (2013) Genetics of ribosomal proteins: "curiouser and curiouser". PLoS Genet 9: e1003300
59. Tsukaya H, Byrne ME, Horiguchi G, Sugiyama M, Van Lijsebettens M, Lenhard M (2013) How do 'housekeeping' genes control organogenesis? Unexpected new findings on the role of housekeeping genes in cell and organ differentiation. J Plant Res 126: 3-15
60. Tucker MR, Okada T, Hu Y, Scholefield A, Taylor JM, Koltunow AM (2012) Somatic small RNA pathways promote the mitotic events of megagametogenesis during female reproductive development in Arabidopsis. Development 139: 1399-1404
61. Tzafrir I, Pena-Muralla R, Dickerman A, Berg M, Rogers R, Hutchens S, Sweeney TC, McElver J, Aux G, Patton D, et al (2004) Identification of genes required for embryo development in Arabidopsis. Plant Physiol 135: 1206-1220
62. Uechi T, Nakajima Y, Nakao A, Torihara H, Chakraborty A, Inoue K, Kenmochi N (2006) Ribosomal protein gene knockdown causes developmental defects in zebrafish. PLoS ONE 1: e37
63. Van Lijsebettens M, Vanderhaeghen R, De Block M, Bauw G, Villarroel R, Van Montagu M (1994) An S18 ribosomal protein gene copy at the Arabidopsis PFL locus affects plant development by its specific expression in meristems. EMBO J 13: 3378-3388
64. Wang SQ, Shi DQ, Long YP, Liu J, Yang WC (2012) GAMETOPHYTE DEFECTIVE 1, a putative subunit of RNases P/MRP, is essential for female gametogenesis and male competence in Arabidopsis. PLoS ONE 7: e33595
65. Warner JR, McIntosh KB (2009) How common are extraribosomal functions of ribosomal proteins? Mol Cell 34: 3-11
66. Watkins-Chow DE, Cooke J, Pidsley R, Edwards A, Slotkin R, Leeds KE, Mullen R, Baxter LL, Campbell TG, Salzer MC, et al (2013) Mutation of the Diamond-Blackfan anemia gene Rps7 in mouse results in morphological and neuroanatomical phenotypes. PLoS Genet 9: e1003094
67. Weijers D, Franke-van Dijk M, Vencken RJ, Quint A, Hooykaas P, Offringa R (2001) An Arabidopsis Minute-like phenotype caused by a semi-dominant mutation in a RIBOSOMAL PROTEIN S5 gene. Development 128: 4289-4299
68. Willig TN, Draptchinskaia N, Dianzani I, Ball S, Niemeyer C, Ramenghi U, Orfali K, Gustavsson P, Garelli E, Brusco A, et al (1999) Mutations in ribosomal protein S19 gene and Diamond Blackfan anemia: wide variations in phenotypic expression. Blood 94: 4294-4306
69. Xue S, Barna M (2012) Specialized ribosomes: a new frontier in gene regulation and organismal biology. Nat Rev Mol Cell Biol 13: 355-369
70. Yao Y, Ling Q, Wang H, Huang H (2008) Ribosomal proteins promote leaf adaxial identity. Development 135: 1325-1334