#PAGE_PARAMS# #ADS_HEAD_SCRIPTS# #MICRODATA#

Mutations on ent-kaurene oxidase 1 encoding gene attenuate its enzyme activity of catalyzing the reaction from ent-kaurene to ent-kaurenoic acid and lead to delayed germination in rice


Autoři: Hui Zhang aff001;  Ming Li aff001;  Dongli He aff001;  Kun Wang aff003;  Pingfang Yang aff001
Působiště autorů: State Key Laboratory of Biocatalysis and Enzyme Engineering, School of Life Sciences, Hubei University, Wuhan, China aff001;  National Key Laboratory of Crop Genetic Improvement and National Centre of Plant Gene Research (Wuhan), Huazhong Agricultural University, Wuhan, China aff002;  School of Life Sciences, Wuhan University, Wuhan, China aff003
Vyšlo v časopise: Mutations on ent-kaurene oxidase 1 encoding gene attenuate its enzyme activity of catalyzing the reaction from ent-kaurene to ent-kaurenoic acid and lead to delayed germination in rice. PLoS Genet 16(1): e32767. doi:10.1371/journal.pgen.1008562
Kategorie: Research Article
doi: https://doi.org/10.1371/journal.pgen.1008562

Souhrn

Rice seed germination is a critical step that determines its entire life circle, with seeds failing to germinate or pre-harvest sprouting both reduce grain yield. Nevertheless, the mechanisms underlying this complex biological event remain unclear. Previously, gibberellin has been shown to promote seed germination. In this study, a delayed seed germination rice mutant was obtained through screening of the EMS induced mutants. Besides of delayed germination, it also shows semi-dwarfism phenotype, which could be recovered by exogenous GA. Through re-sequencing on the mutant, wild-type and their F2 populations, we identified two continuous mutated sites on ent-kaurene oxidase 1 (OsKO1) gene, which result in the conversion from Thr to Met in the cytochrome P450 domain. Genetic complementary analysis and enzyme assay verified that the mutations in OsKO1 gene block the biosynthesis of GA and result in the defect phenotypes. Further analyses proved that OsKO1 could catalyze the reaction from ent-kaurene into ent-kaurenoic acid in GA biosynthesis mainly at seed germination and seedling stages, and the mutations decrease its activity to catalyze the step from ent-kaurenol to ent-kaurenoic acid in this reaction. Transcriptomic and proteomic data indicate that the defect on GA biosynthesis decreases its ability to mobilize starch and attenuate ABA signaling, therefore delay the germination process. The results provide some new insights into both GA biosynthesis and seed germination regulatory pathway in rice.

Klíčová slova:

Biosynthesis – Embryos – Gene expression – Gibberellins – Phenotypes – Rice – Seed germination – Seeds


Zdroje

1. Bewley J. Seed germination and dormancy. Plant Cell. 1997; 9: 1055–1066. doi: 10.1105/tpc.9.7.1055 12237375

2. Wu K, Wang J, Kong Z, Ma ZQ. Characterization of a single recessive yield trait mutant with elevated endogenous ABA concentration and deformed grains, spikelets and leaves. Plant Sci. 2011; 180: 306–312. doi: 10.1016/j.plantsci.2010.10.001 21421375

3. Rajjou L, Duval M, Gallardo K, Catusse J, Bally J, Job C, Job D. Seed germination and vigor. Annu Rev Plant Biol. 2012; 63: 507–533. doi: 10.1146/annurev-arplant-042811-105550 22136565

4. Finkelstein R, Reeves W, Ariizumi T, Steber C. Molecular aspects of seed dormancy. Annu Rev Plant Biol. 2008; 59: 387–415. doi: 10.1146/annurev.arplant.59.032607.092740 18257711

5. Gubler F, Millar AA, Jacobsen JV. Dormancy release, ABA and pre-harvest sprouting. Curr Opin Plant Biol. 2005; 8: 183–187. doi: 10.1016/j.pbi.2005.01.011 15752999

6. Nambara E, Marion-Poll A. ABA action and interactions in seeds. Trends Plant Sci. 2003; 8: 213–217. doi: 10.1016/S1360-1385(03)00060-8 12758038

7. Fang J, Chai C, Qian Q, Li C, Tang J, Sun L, et al. Mutations of genes in synthesis of the carotenoid precursors of ABA lead to pre-harvest sprouting and photo-oxidation in rice. Plant J. 2008; 54: 177–189. doi: 10.1111/j.1365-313X.2008.03411.x 18208525

8. Park GG, Park JJ, Yoon J, Yu SN, An G. A RING finger E3 ligase gene, Oryza sativa Delayed Seed Germination 1 (OsDSG1), controls seed germination and stress responses in rice. Plant Mol Biol. 2010; 74: 467–478. doi: 10.1007/s11103-010-9687-3 20878348

9. Rodriguez P, Benning G, Grill E. ABI2, a second protein phosphatase 2C involved in abscisic acid signal transduction in Arabidopsis. FEBS Lett. 1998; 421: 185–190. doi: 10.1016/s0014-5793(97)01558-5 9468303

10. Zhang X, Garreton V, Chua N-h. The AIP2 E3 ligase acts as a novel negative regulator of ABA signaling by promoting ABI3 degradation. Gene Dev. 2005; 19: 1532–1543. doi: 10.1101/gad.1318705 15998807

11. Ding ZJ, Yan JY, Li GX, Wu ZC, Zhang SQ, Zheng SJ. WRKY41 controls Arabidopsis seed dormancy via direct regulation of ABI3 transcript levels not downstream of ABA. Plant J. 2014; 79: 810–823. doi: 10.1111/tpj.12597 24946881

12. Lopez-Molina L, Mongrand S, Mclachlin DT, Chait BT, Chua N-h. ABI5 acts downstream of ABI3 to execute an ABA-dependent growth arrest during germination. Plant J. 2002; 32: 317–328. doi: 10.1046/j.1365-313x.2002.01430.x 12410810

13. Finkelstein R, Wang M, Lynch T, Rao S, Goodman H. The Arabidopsis abscisic acid response locus ABI4 encodes an APETALA2 domain protein. Plant Cell. 1998; 10: 1043–1054. doi: 10.1105/tpc.10.6.1043 9634591

14. Peng J, Harberd NP. The role of GA-mediated signaling in the control of seed germination. Curr Opin Plant Biol. 2002; 5: 376–381. doi: 10.1016/s1369-5266(02)00279-0 12183174

15. Guo X, Hou X, Fang J, Wei P, Xu B, Chen M, et al. The rice GERMINATION DEFECTIVE 1, encoding a B3 domain transcriptional repressor, regulates seed germination and seedling development by integrating GA and carbohydrate metabolism. Plant J. 2013; 75: 403–416. doi: 10.1111/tpj.12209 23581288

16. Kaneko M, Itoh H, Ueguchi-Tanaka M, Ashikari M, Matsuoka M. The alpha-amylase induction in endosperm during rice seed germination is caused by gibberellin synthesized in epithelium. Plant Physiol. 2002; 128: 1264–1270. doi: 10.1104/pp.010785 11950975

17. Kashem MA, Itoh K, Iwabuchi S, Hori H, Mitsui T. Possible involvement of phosphoinositide-Ca2+ signaling in the regulation of alpha-amylase expression and germination of rice seed (Oryza sativa L.). Plant Cell Physiol. 2000; 41: 399–407. doi: 10.1093/pcp/41.4.399 10845452

18. Tamiru M, Undan JR, Takagi H, Abe A, Yoshida K, Undan JQ, et al. A cytochrome P450, OsDSS1, is involved in growth and drought stress responses in rice (Oryza sativa L.). Plant Mol Biol. 2015; 88: 85–99. doi: 10.1007/s11103-015-0310-5 25800365

19. Chen X, Wu Y, Guo J, Du B, Chen R, Zhu L, He G. A rice lectin receptor-like kinase that is involved in innate immune responses also contributes to seed germination. Plant J. 2013; 76: 687–698. doi: 10.1111/tpj.12328 24033867

20. Ye H, Feng J, Zhang L, Zhang J, Mispan MS, Cao Z, et al. Map-based cloning of seed dormancy1-2 identified a gibberellin synthesis gene regulating the development of endosperm-imposed dormancy in rice. Plant Physiol. 2015; 169: 2152–2165. doi: 10.1104/pp.15.01202 26373662

21. Aach H, Bode H, Robinson DG, Graebe JE. ent-Kaurene synthase is located in proplastids of meristematic shoot tissues. Planta. 1996; 202: 211–219.

22. Helliwell CA, Sullivan JA, Mould RM, Gray JC, Peacock WJ, Dennis ES. A plastid envelope location of Arabidopsis ent-Kaurene oxidase links the plastid and endoplasmic reticulum steps of the gibberellin biosynthesis. Plant J. 2001; 28: 201–208. doi: 10.1046/j.1365-313x.2001.01150.x 11722763

23. Sakamoto T, Miura K, Itoh H, Tatsumi T, Ueguchi-Tanaka M, Ishiyama K, et al. An overview of gibberellin metabolism enzyme genes and their related mutants in rice. Plant Physiol. 2004; 134: 1642–1653. doi: 10.1104/pp.103.033696 15075394

24. Yamaguchi S. Gibberellin metabolism and its regulation. Annu Rev Plant Biol. 2008; 59: 225–251. doi: 10.1146/annurev.arplant.59.032607.092804 18173378

25. Magome H, Nomura T, Hanada A, Takeda-Kamiya N, Ohnishi T, Shinma Y, et al. CYP714B1 and CYP714B2 encode gibberellin 13-oxidases that reduce gibberellin activity in rice. Proc Natl Acad Sci USA. 2013; 110: 1947–1952. doi: 10.1073/pnas.1215788110 23319637

26. Itoh H, Tatsumi T, Sakamoto T, Otomo K, Toyomasu T, Kitano H, et al. A rice semi-dwarf gene, Tan-Ginbozu (D35), encodes the gibberellin biosynthesis enzyme, ent-kaurene oxidase. Plant Mol Biol. 2004; 54: 533–547. doi: 10.1023/B:PLAN.0000038261.21060.47 15316288

27. Ko K-W, Lin F, Katsumata T, Sugai Y, Miyazaki S, Kawaide H, et al. Functional identification of a rice ent-kaurene oxidase, OsKO2, using the Pichia pastoris expression system. Biosci Biotech Bioch. 2014; 72: 3285–3288.

28. Li J, Jiang J, Qian Q, Xu Y, Zhang C, Xiao J, et al. Mutation of Rice BC12/GDD1, Which Encodes a Kinesin-Like Protein That Binds to a GA Biosynthesis Gene Promoter, Leads to Dwarfism with Impaired Cell Elongation. Plant Cell. 2011; 23: 628–640. doi: 10.1105/tpc.110.081901 21325138

29. Chen X, Tian X, Xue L, Zhang X, Yang S, Traw MB, Huang J. CRISPR-Based Assessment of Gene Specialization in the Gibberellin Metabolic Pathway in Rice. Plant Physiol. 2019; 180: 2091–2105. doi: 10.1104/pp.19.00328 31160507

30. Helliwell CA, Chandler PM, Poole A, Dennis ES, Peacock WJ. The CYP88A cytochrome P450, ent-kaurenoic acid oxidase, catalyzes three steps of the gibberellin biosynthesis pathway. Proc Natl Acad Sci USA. 2001; 98: 2065–2070. doi: 10.1073/pnas.041588998 11172076

31. Magome H, Yamaguchi S, Hanada A, Kamiya Y, Oda K. Dwarf and delayed-flowering 1, a novel Arabidopsis mutant deficient in gibberellin biosynthesis because of overexpression of a putative AP2 transcription factor. Plant J. 2004; 37: 720–729. doi: 10.1111/j.1365-313x.2003.01998.x 14871311

32. Margis-Pinheiro M, Zhou XR, Zhu QH, Dennis ES, Upadhyaya NM. Isolation and characterization of a Ds-tagged rice (Oryza sativa L.) GA-responsive dwarf mutant defective in an early step of the gibberellin biosynthesis pathway. Plant Cell Rep. 2005; 23: 819–833. doi: 10.1007/s00299-004-0896-6 15668792

33. Sponsel VM, Schmidt FW, Porter SG, Nakayama M, Kohlstruk S, Estelle M. Characterization of new gibberellin-Responsive semidwarf mutants of Arabidopsis. Plant Physiol. 1997; 115: 1009–1020. doi: 10.1104/pp.115.3.1009 9390435

34. Denisov IG, Makris TM, Sligar SG, Schlichting I. Structure and chemistry of cytochrome P450. Chem Rev. 2005; 105: 2253–2278. doi: 10.1021/cr0307143 15941214

35. Toyomasu T, Usui M, Sugawara C, Kanno Y, Sakai A, Takahashi H, et al. Transcripts of two ent-copalyl diphosphate synthase genes differentially localize in rice plants according to their distinct biological roles. J Exp Bot. 2014; 66: 369–376. doi: 10.1093/jxb/eru424 25336684

36. He D, Han C, Yao J, Shen S, Yang P. Constructing the metabolic and regulatory pathways in germinating rice seeds through proteomic approach. Proteomics. 2011; 11: 2693–2713. doi: 10.1002/pmic.201000598 21630451

37. Lefebvre V, North H, Frey A, Sotta B, Seo M, Okamoto M, et al. Functional analysis of Arabidopsis NCED6 and NCED9 genes indicates that ABA synthesized in the endosperm is involved in the induction of seed dormancy. Plant J. 2006; 45: 309–319. doi: 10.1111/j.1365-313X.2005.02622.x 16412079

38. Nambara E, Marion-Poll A. Abscisic acid biosynthesis and catabolism. Annu Rev Plant Biol. 2005; 56: 165–185. doi: 10.1146/annurev.arplant.56.032604.144046 15862093

39. Saika H, Okamoto M, Miyoshi K, Kushiro T, Shinoda S, Jikumaru Y, et al. Ethylene promotes submergence-induced expression of OsABA8ox1, a gene that encodes ABA 8' -hydroxylase in rice. Plant Cell Physiol. 2007; 48: 287–298. doi: 10.1093/pcp/pcm003 17205969

40. Song SY, Dai XY, Zhang W-H. A rice F-box gene, OsFbx352, is involved in glucose-delayed seed germination in rice. J Exp Bot. 2012; 63: 5559–5568. doi: 10.1093/jxb/ers206 22859682

41. Debeaujon I, Koornneef M. Gibberellin requirement for Arabidopsis seed germination is determined both by testa characteristics and embryonic abscisic acid. Plant Physiol. 2000; 122: 415–424. doi: 10.1104/pp.122.2.415 10677434

42. Ogawa M, Hanada A, Yamauchi Y, Kuwahara A, Kamiya Y, Yamaguchi S. Gibberellin biosynthesis and response during Arabidopsis seed germination. Plant Cell. 2003; 15: 1591–1604. doi: 10.1105/tpc.011650 12837949

43. Piskurewicz U, Jikumaru Y, Kinoshita N, Nambara E, Kamiya Y, Lopez-Molina L. The gibberellic acid signaling repressor RGL2 inhibits Arabidopsis seed germination by stimulating abscisic acid synthesis and ABI5 activity. Plant Cell. 2008; 20: 2729–2745. doi: 10.1105/tpc.108.061515 18941053

44. Wu J, Zhu C, Pang J, Zhang X, Yang C, Xia G, et al. OsLOL1, a C2C2-type zinc finger protein, interacts with OsbZIP58 to promote seed germination through the modulation of gibberellin biosynthesis in Oryza sativa. Plant J. 2014; 80: 1118–1130. doi: 10.1111/tpj.12714 25353370

45. Wang Q, Hillwig ML, Wu Y, Peters RJ. CYP701A8: a rice ent-kaurene oxidase paralog diverted to more specialized diterpenoid metabolism. Plant Physiol. 2012; 158: 1418–1425. doi: 10.1104/pp.111.187518 22247270

46. Zhu S, Gao F, Cao X, Chen M, Ye G, Wei C, Li Y. The rice dwarf virus P2 protein interacts with ent-kaurene oxidases in vivo, leading to reduced biosynthesis of gibberellins and rice dwarf symptoms. Plant Physiol. 2005; 139: 1935–1945. doi: 10.1104/pp.105.072306 16299167

47. White CN, Rivin CJ. Gibberellins and Seed Development in Maize. II. Gibberellin synthesis inhibition enhances Abscisic Acid signaling in cultured embryos. Plant Physiol. 2000; 122: 1089–1097. doi: 10.1104/pp.122.4.1089 10759504

48. Khurana P, Vishnudasan D, Chhibbar AK. Genetic approaches towards overcoming water deficit in plants-special emphasis on LEAs. Physiol Mol Biol Plants. 2008; 14: 277–297. doi: 10.1007/s12298-008-0026-y 23572894

49. Lu G, Gao C, Zheng X, Han B. Identification of OsbZIP72 as a positive regulator of ABA response and drought tolerance in rice. Planta. 2009; 229: 605–615. doi: 10.1007/s00425-008-0857-3 19048288

50. Nguyen TP, Cueff G, Hegedus DD, Rajjou L, Bentsink L. A role for seed storage proteins in Arabidopsis seed longevity. J Exp Bot. 2015; 66: 6399–6413. doi: 10.1093/jxb/erv348 26184996

51. Yazaki J, Kikuchi S. The Genomic View of Genes Responsive to the Antagonistic Phytohormones, Abscisic Acid, and Gibberellin. Vitam Horm. 2005; 72: 1–30. doi: 10.1016/S0083-6729(05)72001-X 16492467

52. Yang P, Li X, Wang X, Chen H, Chen F, Shen S. Proteomic analysis of rice (Oryza sativa) seeds during germination. Proteomics. 2007; 7: 3358–3368. doi: 10.1002/pmic.200700207 17849412

53. Fincher GB. Molecular and cellular biology associated with endosperm mobilization in germinating cereal grains. Annu Rev Plant Physiol Plant Mol Biol. 1989; 40: 305–346.

54. Zhao L, Hu Y, Chong K, Wang T. ARAG1, an ABA-responsive DREB gene, plays a role in seed germination and drought tolerance. Ann Bot-London. 2010; 105: 401–409.

55. Dai C, Xue HW. Rice early flowering1, a CKI, phosphorylates DELLA protein SLR1 to negatively regulate gibberellin signalling. EMBO J. 2010; 29: 1916–1927. doi: 10.1038/emboj.2010.75 20400938

56. Hirano K, Kouketu E, Katoh H, Aya K, Ueguchi-Tanaka M, Matsuoka M. The suppressive function of the rice DELLA protein SLR1 is dependent on its transcriptional activation activity. Plant J. 2012; 71: 443–453. doi: 10.1111/j.1365-313X.2012.05000.x 22429711

57. Sasaki A, Itoh H, Gomi K, Ueguchi-Tanaka M, Ishiyama K, Kobayashi M, et al. Accumulation of phosphorylated repressor for gibberellin signaling in an F-box mutant. Science. 2003; 299: 1896–1898. doi: 10.1126/science.1081077 12649483

58. Takagi H, Uemura A, Yaegashi H, Tamiru M, Abe A, Mitsuoka C, et al. MutMap-Gap: whole-genome resequencing of mutant F2 progeny bulk combined with de novo assembly of gap regions identifies the rice blast resistance gene Pii. New Phytol. 2013; 200: 276–283. doi: 10.1111/nph.12369 23790109

59. Li H, Durbin R. Fast and accurate short read alignment with Burrows-Wheeler Transform. Bioinformatics. 2009; 25: 1754–1760. doi: 10.1093/bioinformatics/btp324 19451168

60. Kawahara Y, Bastide M, Hamilton J, Kanamori H, Mccombie W, Ouyang S, et al. Improvement of the Oryza sativa Nipponbare reference genome using next generation sequence and optical map data. Rice. 2013; 6: 1–10. doi: 10.1186/1939-8433-6-1

61. Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, et al. The sequence alignment/map format and samtools. Bioinformatics. 2009; 25: 2078–2079. doi: 10.1093/bioinformatics/btp352 19505943

62. McKenna A, Hanna M, Banks E, Sivachenko A, Cibulskis K, Kernytsky A, et al. The genome analysis toolkit: a mapreduce framework for analyzing next-generation DNA sequencing data. Genome Res. 2010; 20: 1297–1303. doi: 10.1101/gr.107524.110 20644199

63. Abe A, Kosugi S, Yoshida K, Natsume S, Takagi H, Kanzaki H, et al. Genome sequencing reveals agronomically important loci in rice using MutMap. Nat Biotechnol. 2012; 30: 174–178. doi: 10.1038/nbt.2095 22267009

64. Billard A, Laval V, Fillinger S, Leroux P, Lachaise H, Beffa R, Debieu D. The allele-specific probe and primer amplification assay, a new real-time PCR method for fine quantification of single-nucleotide polymorphisms in pooled DNA. Appl Environ Microb. 2012; 78: 1063–1068.

65. Hui L, DelMonte T, Ranade K. Genotyping Using the Taqman Assay. Curr Protoc Hum Genet. 2008; 56: 2.10.1–2.10.8.

66. Hiei Y, Ohta S, Komari T, Kumashiro T. Efficient transformation of rice (Oryza sativa L.) mediated by Agrobasterium and sequence analysis of boundaries of the T-DNA. Plant J. 1994; 6: 271–282. doi: 10.1046/j.1365-313x.1994.6020271.x 7920717

67. Chen ML, Fu XM, Liu JQ, Ye TT, Hou SY, Huang YQ, et al. Highly sensitive and quantitative profiling of acidic phytohormones using derivatization approach coupled with nano-LC-ESI-Q-TOF-MS analysis. J Chromatogr B. 2012; 905: 67–74.

68. Liu Y, Liu M, Li X, Cao B, Ma X. Identification of differentially expressed genes in leaf of Reaumuria soongorica under PEG-induced drought stress by digital gene expression profiling. PloS one. 2014; 9: e94277. doi: 10.1371/journal.pone.0094277 24736242

69. Yang C, Jiang M, Wen H, Tian J, Liu W, Wu F, Gou G. Analysis of differential gene expression under low-temperature stress in Nile tilapia (Oreochromis niloticus) using digital gene expression. Gene. 2015; 564: 134–140. doi: 10.1016/j.gene.2015.01.038 25617524

70. Trapnell C, Williams BA, Pertea G, Mortazavi A, Kwan G, van Baren MJ, et al. Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation. Nat Biotechnol. 2010; 28: 511–515. doi: 10.1038/nbt.1621 20436464

71. Li M, Wang K, Wang X, Yang P. Morphological and proteomic analysis reveal the role of pistil under pollination in Liriodendron chinense (Hemsl.) Sarg. PloS one 2014; 9: e99970. doi: 10.1371/journal.pone.0099970 24924488

72. Li M, Sha A, Zhou X, Yang P. Comparative proteomic analyses reveal the changes of metabolic features in soybean (Glycine max) pistils upon pollination. Sex Plant Reprod. 2012; 25: 281–291. doi: 10.1007/s00497-012-0197-0 22968406

73. Yoo SD, Cho YH, Sheen J. Arabidopsis mesophyll protoplasts: a versatile cell system for transient gene expression analysis. Nat Protoc. 2007; 2: 1565–1572. doi: 10.1038/nprot.2007.199 17585298

Štítky
Genetika Reprodukční medicína

Článek vyšel v časopise

PLOS Genetics


2020 Číslo 1
Nejčtenější tento týden
Nejčtenější v tomto čísle
Kurzy

Zvyšte si kvalifikaci online z pohodlí domova

KOST
Koncepce osteologické péče pro gynekology a praktické lékaře
nový kurz
Autoři: MUDr. František Šenk

Sekvenční léčba schizofrenie
Autoři: MUDr. Jana Hořínková

Hypertenze a hypercholesterolémie – synergický efekt léčby
Autoři: prof. MUDr. Hana Rosolová, DrSc.

Svět praktické medicíny 5/2023 (znalostní test z časopisu)

Imunopatologie? … a co my s tím???
Autoři: doc. MUDr. Helena Lahoda Brodská, Ph.D.

Všechny kurzy
Kurzy Podcasty Doporučená témata Časopisy
Přihlášení
Zapomenuté heslo

Zadejte e-mailovou adresu, se kterou jste vytvářel(a) účet, budou Vám na ni zaslány informace k nastavení nového hesla.

Přihlášení

Nemáte účet?  Registrujte se

#ADS_BOTTOM_SCRIPTS#