Genetic analysis and fine mapping of a qualitative trait locus wpb1 for albino panicle branches in rice

English version

Autoři: Zhongquan Cai ^aff001; Peilong Jia ^aff002; Jiaqiang Zhang ^aff003; Ping Gan ^aff001; Qi Shao ^aff001; Gang Jin ^aff004; Liping Wang ^aff004; Jian Jin ^aff001; Jiangyi Yang ^aff001; Jijing Luo ^aff001
Působiště autorů: College of Life Science and Technology, State Key Laboratory for Conservation and Utilization of Subtropical Agro-Bioresources, Guangxi University, Nanning, China ^aff001; Institute for New Rural Development, National Demonstration Center for Experimental Plant Science Education, College of Agriculture, Guangxi University, Nanning, Guangxi, China ^aff002; Research and Development Centre of Flower, Zhejiang Academy of Agricultural Sciences, Hangzhou, China ^aff003; Guangxi Subtropical Crops Research Institute, Nanning, China ^aff004
Vyšlo v časopise: PLoS ONE 14(9)
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pone.0223228

Souhrn

Chloroplast plays an important role in the plant life cycle. However, the details of its development remain elusive in rice. In this study, we report the fine-mapping of a novel rice gene wpb1 (white panicle branch 1), which affects chloroplast biogenesis, from a tropical japonica variety that results in an albino panicle branches at and after the heading stage. The wpb1 variety was crossed with Nipponbare to generate the F₂ and BC₁F₂ populations. Green and white panicle branch phenotypes with a 3:1 segregation ratio was observed in the F₂ population. Bulked segregant analysis (BSA) based on whole genome resequencing was conducted to determine the wpb1 locus. A candidate interval spanning from 11.35 to 23.79M (physical position) on chromosome 1 was identified. The results of BSA analysis were verified by a 40K rice SNP-array using the BC₁F₂ population. A large-scale F₂ population was used to pinpoint wpb1, and the locus was further narrowed down to a 95-kb interval. Furthermore, our results showed that the expression levels of the majority of the genes involved in Chl biosynthesis, photosynthesis and chloroplast development were remarkably affected in wpb1 variety and in F₂ plants with a white panicle branch phenotype. In line with the results mentioned above, anatomical structural examination and chlorophyll (Chl) content measurement suggested that wpb1 might play an important role in the regulation of chloroplast development. Further cloning and functional characterization of the wpb1 gene will shed light on the molecular mechanism underlying chloroplast development in rice.

Klíčová slova:

Rice – Genetic loci – Biosynthesis – Leaves – Photosynthesis – Chloroplasts – Chlorophyll – Panicles

Zdroje

1. Fromme P, Melkozernov A, Jordan P, Krauss N. Structure and function of photosystem I: interaction with its soluble electron carriers and external antenna systems. FEBS letters. 2003;555(1):40–4. Epub 2003/11/25. doi: 10.1016/s0014-5793(03)01124-4 14630316.

2. Breinholt V, Schimerlik M, Dashwood R, Bailey G. Mechanisms of chlorophyllin anticarcinogenesis against aflatoxin B1: complex formation with the carcinogen. Chemical research in toxicology. 1995;8(4):506–14. Epub 1995/06/01. 7548730.

3. Wicke S, Schneeweiss GM, dePamphilis CW, Muller KF, Quandt D. The evolution of the plastid chromosome in land plants: gene content, gene order, gene function. Plant molecular biology. 2011;76(3–5):273–97. Epub 2011/03/23. doi: 10.1007/s11103-011-9762-4 21424877; PubMed Central PMCID: PMC3104136.

4. Kusumi K, Mizutani A, Nishimura M, Iba K. A virescent gene V1 determines the expression timing of plastid genes for transcription/translation apparatus during early leaf development in rice. The Plant Journal. 1997;12(6):1241–50. doi: 10.1046/j.1365-313x.1997.12061241.x

5. Kusumi K, Komori H, Satoh H, Iba K. Characterization of a zebra mutant of rice with increased susceptibility to light stress. Plant & cell physiology. 2000;41(2):158–64. Epub 2000/05/05. doi: 10.1093/pcp/41.2.158 10795309.

6. Sugimoto H, Kusumi K, Noguchi K, Yano M, Yoshimura A, Iba K. The rice nuclear gene, VIRESCENT 2, is essential for chloroplast development and encodes a novel type of guanylate kinase targeted to plastids and mitochondria. The Plant journal: for cell and molecular biology. 2007;52(3):512–27. Epub 2007/08/31. doi: 10.1111/j.1365-313X.2007.03251.x 17727616.

7. Golden SS, Brusslan J, Haselkorn R. Expression of a family of psbA genes encoding a photosystem II polypeptide in the cyanobacterium Anacystis nidulans R2. The EMBO journal. 1986;5(11):2789–98. Epub 1986/11/01. 3098559; PubMed Central PMCID: PMC1167224.

8. Sundberg E, Slagter JG, Fridborg I, Cleary SP, Robinson C, Coupland G. ALBINO3, an Arabidopsis nuclear gene essential for chloroplast differentiation, encodes a chloroplast protein that shows homology to proteins present in bacterial membranes and yeast mitochondria. The Plant Cell. 1997;9:717–30. doi: 10.1105/tpc.9.5.717 9165749

9. Zhou K, Ren Y, Lv J, Wang Y, Liu F, Zhou F, et al. Young Leaf Chlorosis 1, a chloroplast-localized gene required for chlorophyll and lutein accumulation during early leaf development in rice. Planta. 2013;237(1):279–92. doi: 10.1007/s00425-012-1756-1 23053539

10. Bae CH, Abe T, Matsuyama T, Fukunishi N, Nagata N, Nakano T, et al. Regulation of chloroplast gene expression is affected in ali, a novel tobacco albino mutant. Ann Bot. 2001;88(4):545–53. doi: 10.1006/anbo.2001.1495 WOS:000171549300004.

11. Hou DY, Xu H, Du GY, Lin JT, Duan M, Guo AG. Proteome analysis of chloroplast proteins in stage albinism line of winter wheat (triticum aestivum) FA85. BMB reports. 2009;42(7):450–5. Epub 2009/08/01. doi: 10.5483/bmbrep.2009.42.7.450 19643044.

12. Schmitz-Linneweber C, Williams-Carrier RE, Williams-Voelker PM, Kroeger TS, Vichas A, Barkan A. A pentatricopeptide repeat protein facilitates the trans-splicing of the maize chloroplast rps12 pre-mRNA. Plant Cell. 2006;18(10):2650–63. Epub 2006/10/17. doi: 10.1105/tpc.106.046110 17041147; PubMed Central PMCID: PMC1626628.

13. Li L, Xiong Y, Ouyang L, Peng X, Chen X, He X, et al. Identification and gene mapping of white stripe leaf and white panicle mutant wlp6 in rice. Chinese Journal of Rice Science. 2018;32(6):538–48. doi: 10.16819/j.1001-7216.2018.7144

14. Yoo SC, Cho SH, Sugimoto H, Li J, Kusumi K, Koh HJ, et al. Rice virescent3 and stripe1 encoding the large and small subunits of ribonucleotide reductase are required for chloroplast biogenesis during early leaf development. Plant physiology. 2009;150(1):388–401. Epub 2009/03/20. doi: 10.1104/pp.109.136648 19297585; PubMed Central PMCID: PMC2675711.

15. Kusumi K, Sakata C, Nakamura T, Kawasaki S, Yoshimura A, Iba K. A plastid protein NUS1 is essential for build-up of the genetic system for early chloroplast development under cold stress conditions. The Plant journal: for cell and molecular biology. 2011;68(6):1039–50. Epub 2011/10/11. doi: 10.1111/j.1365-313X.2011.04755.x 21981410.

16. Dong H, Fei GL, Wu CY, Wu FQ, Sun YY, Chen MJ, et al. A rice virescent-yellow leaf mutant reveals new insights into the role and assembly of plastid caseinolytic protease in higher plants. Plant Physiol. 2013;162(4):1867–80. doi: 10.1104/pp.113.217604 23803583; PubMed Central PMCID: PMC3729767.

17. Sugimoto H, Kusumi K, Tozawa Y, Yazaki J, Kishimoto N, Kikuchi S, et al. The virescent-2 mutation inhibits translation of plastid transcripts for the plastid genetic system at an early stage of chloroplast differentiation. Plant & cell physiology. 2004;45(8):985–96. Epub 2004/09/10. doi: 10.1093/pcp/pch111 15356324.

18. Tan J, Tan Z, Wu F, Sheng P, Heng Y, Wang X, et al. A Novel Chloroplast-Localized Pentatricopeptide Repeat Protein Involved in Splicing Affects Chloroplast Development and Abiotic Stress Response in Rice. Molecular Plant. 2014;7(8):1329–49. doi: 10.1093/mp/ssu054 24821718

19. Wang Y, Ren Y, Zhou K, Liu L, Wang J, Xu Y, et al. WHITE STRIPE LEAF4 Encodes a Novel P-Type PPR Protein Required for Chloroplast Biogenesis during Early Leaf Development. Frontiers in plant science. 2017;8:1116. Epub 2017/07/12. doi: 10.3389/fpls.2017.01116 28694820; PubMed Central PMCID: PMC5483476.

20. Wang L, Wang C, Wang Y, Niu M, Ren Y, Zhou K, et al. WSL3, a component of the plastid-encoded plastid RNA polymerase, is essential for early chloroplast development in rice. Plant molecular biology. 2016;92(4–5):1–15.

21. Zhou K, Ren Y, Feng Z, Ying W, Long Z, Jia L, et al. Young Seedling Stripe1 encodes a chloroplast nucleoid-associated protein required for chloroplast development in rice seedlings. Planta. 2017;245(1):45–60. doi: 10.1007/s00425-016-2590-7 27578095

22. Sanchez AC, Khush GS. Chromosomal location of some marker genes in rice using the primary trisomics. Journal of Heredity. 1994;85(4):297–300.

23. Wang Y, Wang C, Zheng M, Lyu J, Xu Y, Li X, et al. WHITE PANICLE1, a Val-tRNA Synthetase Regulating Chloroplast Ribosome Biogenesis in Rice, Is Essential for Early Chloroplast Development. Plant physiology. 2016;170(4):2110–23. Epub 2017/10/19. doi: 10.1093/jxb/erx332 10.1104/pp.15.01949. 26839129.

24. Chen Y. Genetic Analysis and Fine Mapping of Gene in Mutant Rice With Stripe White Leaf and White Panicle. Journal of Nuclear Agricultural Sciences. 2015;29(7):1246–52.

25. Kunneng Z, Jiafa X, Tingchen MA, Yuanlei W, Zefu LI. Mapping and Mutation Analysis of Stripe Leaf and White Panicle Gene SLWP in Rice. Chinese Journal of Rice Science. 2018;32(4):325–34.

26. Zeng Y, Wei X, Rui Z, Huang J, Xu X. Agronomic Character Analysis and Gene Mapping of An Albino Mutant in Rice. Molecular Plant Breeding. 2018;16(6):1955–61.

27. Chen DX, Ting LI, Guang-Lin QU, Huang WJ, Zhong-Quan HE, Shi-Gui LI. Characterization and Genetic Analysis of a Streaked and Abnormal Glumous Flower Mutant st-fon. Chinese Journal of Rice Science. 2012;26(6):677–85.

28. Wang XW, Jiang YD, Liao HX, Bo Y, Zou SY, Zhu XY, et al. Identification and Gene Fine Mapping of White Panicle Mutant wp4 in Oryza sativa. Acta Agronomica Sinica. 2015;41(6):838–44.

29. Song J, Wei X, Shao G, Sheng Z, Chen D, Liu C, et al. The rice nuclear gene WLP1 encoding a chloroplast ribosome L13 protein is needed for chloroplast development in rice grown under low temperature conditions. Plant molecular biology. 2014;84(3):301–14. doi: 10.1007/s11103-013-0134-0 24132771

30. Jin Y, Liu HQ, Wang YZ. Genetic Analysis and Gene Mapping of a White Striped Leaf and White Panicle Mutant in Rice. Chinese Journal of Rice Science. 2011;25(5):461–6.

31. Zhang Z, Cui X, Wang Y, Wu J, Gu X, Lu T. The RNA Editing Factor WSP1 Is Essential for Chloroplast Development in Rice. Mol Plant. 2017;10(1):86–98. Epub 2016/09/14. doi: 10.1016/j.molp.2016.08.009 27622591.

32. Michelmore RW, Paran I, Kesseli RV. Identification of markers linked to disease-resistance genes by bulked segregant analysis: a rapid method to detect markers in specific genomic regions by using segregating populations. Proceedings of the National Academy of Sciences of the United States of America. 1991;88(21):9828–32. Epub 1991/11/01. doi: 10.1073/pnas.88.21.9828 1682921; PubMed Central PMCID: PMC52814.

33. Takagi H, Abe A, Yoshida K, Kosugi S, Natsume S, Mitsuoka C, et al. QTL-seq: rapid mapping of quantitative trait loci in rice by whole genome resequencing of DNA from two bulked populations. Plant J. 2013;74(1):174–83. doi: 10.1111/tpj.12105 23289725.

34. Schneeberger K, Ossowski S, Lanz C, Juul T, Petersen AH, Nielsen KL, et al. SHOREmap: simultaneous mapping and mutation identification by deep sequencing. Nature methods. 2009;6(8):550–1. Epub 2009/08/01. doi: 10.1038/nmeth0809-550 19644454.

35. Sun J, Yang L, Wang J, Liu H, Zheng H, Xie D, et al. Identification of a cold-tolerant locus in rice (Oryza sativa L.) using bulked segregant analysis with a next-generation sequencing strategy. Rice (New York, NY). 2018;11(1):24–. doi: 10.1186/s12284-018-0218-1 29671148.

36. Abe A, Kosugi S, Yoshida K, Natsume S, Takagi H, Kanzaki H, et al. Genome sequencing reveals agronomically important loci in rice using MutMap. Nature biotechnology. 2012;30(2):174–8. Epub 2012/01/24. doi: 10.1038/nbt.2095 22267009.

37. Klein H, Xiao Y, Conklin PA, Govindarajulu R, Kelly JA, Scanlon MJ, et al. Bulked-Segregant Analysis Coupled to Whole Genome Sequencing (BSA-Seq) for Rapid Gene Cloning in Maize. G3: Genes|Genomes|Genetics. 2018;8:3583–92. doi: 10.1534/g3.118.200499 30194092

38. Li H, Durbin R. Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics (Oxford, England). 2009;25(14):1754–60. Epub 2009/05/20. doi: 10.1093/bioinformatics/btp324 19451168; PubMed Central PMCID: PMC2705234.

39. 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 research. 2010;20(9):1297–303. Epub 2010/07/21. doi: 10.1101/gr.107524.110 20644199; PubMed Central PMCID: PMC2928508.

40. Wang K, Li M, Hakonarson H. ANNOVAR: functional annotation of genetic variants from high-throughput sequencing data. Nucleic acids research. 2010;38(16):e164. Epub 2010/07/06. doi: 10.1093/nar/gkq603 20601685; PubMed Central PMCID: PMC2938201.

41. Lin D, Jiang Q, Zheng K, Chen S, Zhou H, Gong X, et al. Mutation of the rice ASL2 gene encoding plastid ribosomal protein L21 causes chloroplast developmental defects and seedling death. Plant Biology. 2015;17(3):599–607. doi: 10.1111/plb.12271 25280352

42. Hiratsuka J, Shimada H, Whittier R, Ishibashi T, Sakamoto M, Mori M, et al. The complete sequence of the rice (Oryza sativa) chloroplast genome: intermolecular recombination between distinct tRNA genes accounts for a major plastid DNA inversion during the evolution of the cereals. Molecular & general genetics: MGG. 1989;217(2–3):185–94. Epub 1989/06/01. doi: 10.1007/bf02464880 2770692.

43. Kyozuka J, McElroy D, Hayakawa T, Xie Y, Wu R, Shimamoto K. Light-regulated and cell-specific expression of tomato rbcS-gusA and rice rbcS-gusA fusion genes in transgenic rice. Plant physiology. 1993;102(3):991–1000. Epub 1993/07/01. doi: 10.1104/pp.102.3.991 8278540; PubMed Central PMCID: PMC158873.

44. Wu Z, Zhang X, He B, Diao L, Sheng S, Wang J, et al. A chlorophyll-deficient rice mutant with impaired chlorophyllide esterification in chlorophyll biosynthesis. Plant physiology. 2007;145(1):29–40. Epub 2007/05/31. doi: 10.1104/pp.107.100321 17535821; PubMed Central PMCID: PMC1976586.

45. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods (San Diego, Calif). 2001;25(4):402–8. Epub 2002/02/16. doi: 10.1006/meth.2001.1262 11846609.

46. Qiu N, Wang X, Yang F, Yang X, Wen Y, Diao R, et al. Fast Extraction and Precise Determination of Chlorophyll. Chinese Bulletin of Botany. 2016;51(5):667–78.

47. Su N, Hu ML, Wu DX, Wu FQ, Fei GL, Lan Y, et al. Disruption of a rice pentatricopeptide repeat protein causes a seedling-specific albino phenotype and its utilization to enhance seed purity in hybrid rice production. Plant physiology. 2012;159(1):227–38. Epub 2012/03/21. doi: 10.1104/pp.112.195081 22430843; PubMed Central PMCID: PMC3366715.

48. Hayashi-Tsugane M, Takahara H, Ahmed N, Himi E, Takagi K, Iida S, et al. A mutable albino allele in rice reveals that formation of thylakoid membranes requires the SNOW-WHITE LEAF1 gene. Plant & cell physiology. 2014;55(1):3–15. Epub 2013/10/24. doi: 10.1093/pcp/pct149 24151203.

49. Liu C, Zhu H, Xing Y, Tan J, Chen X, Zhang J, et al. Albino Leaf 2 is involved in the splicing of chloroplast group I and II introns in rice. Journal of experimental botany. 2016;67(18):5339–47. Epub 2016/08/21. doi: 10.1093/jxb/erw296 27543605; PubMed Central PMCID: PMC5049385.

50. Zhang Z, Tan J, Shi Z. Albino Leaf1 That Encodes the Sole Octotricopeptide Repeat Protein Is Responsible for Chloroplast Development. Plant physiology. 2016;171(2):1182–91. doi: 10.1104/pp.16.00325 27208287.

51. Lv Y, Shao G, Qiu J, Jiao G, Sheng Z, Xie L, et al. White Leaf and Panicle 2, encoding a PEP-associated protein, is required for chloroplast biogenesis under heat stress in rice. J Exp Bot. 2017;68(18):5147–60. Epub 2017/10/19. doi: 10.1093/jxb/erx332 29045742; PubMed Central PMCID: PMC5853965.

52. Zeng X, Tang R, Guo H, Ke S, Teng B, Hung YH, et al. A naturally occurring conditional albino mutant in rice caused by defects in the plastid-localized OsABCI8 transporter. Plant molecular biology. 2017;94(1–2):137–48. Epub 2017/03/13. doi: 10.1007/s11103-017-0598-4 28285416.

53. Zhang T, Feng P, Li Y, Yu P, Yu G, Sang X, et al. VIRESCENT-ALBINO LEAF 1 regulates leaf colour development and cell division in rice. Journal of experimental botany. 2018;69(20):4791–804. Epub 2018/08/14. doi: 10.1093/jxb/ery250 30102358; PubMed Central PMCID: PMC6137968.

54. Iwata Omura NaT. Linkage studies in rice (Oryza sativa L.). Some albino genes and their linkage relation with marker genes. Sci Bull Fac Agr Kyushu Univ. 1978;33(1):11–8.

55. Gong X, Jiang Q, Xu J, Zhang J, Teng S, Lin D, et al. Disruption of the rice plastid ribosomal protein S20 leads to chloroplast developmental defects and seedling lethality. G3: Genes Genomes Genetics. 2013;3(10):1769–77. doi: 10.1534/g3.113.007856 23979931

56. Lin D, Gong X, Jiang Q, Zheng K, Zhou H, Xu J, et al. The rice ALS3 encoding a novel pentatricopeptide repeat protein is required for chloroplast development and seedling growth. Rice (New York, NY). 2015;8:17-. doi: 10.1186/s12284-015-0050-9 25859292.

57. Li H, Ji G, Wang Y, Qian Q, Xu J, Sodmergen, et al. WHITE PANICLE3, a Novel Nucleus-Encoded Mitochondrial Protein, Is Essential for Proper Development and Maintenance of Chloroplasts and Mitochondria in Rice. Frontiers in plant science. 2018;9:762–. doi: 10.3389/fpls.2018.00762 29928286.

58. van Wijk KJ, Baginsky S. Plastid proteomics in higher plants: current state and future goals. Plant Physiol. 2011;155(4):1578–88. Epub 2011/02/26. doi: 10.1104/pp.111.172932 21350036; PubMed Central PMCID: PMC3091083.

Genetic analysis and fine mapping of a qualitative trait locus wpb1 for albino panicle branches in rice

Souhrn

Klíčová slova:

Zdroje

PLOS One

Aktuální možnosti diagnostiky a léčby litiáz