The OsGATA gene family as a promising candidate for applying the CRISPR/Cas genome editing technology to improve the nutritional and yield qualities of rice (Oryza sativa L.)

Molecular breeding of rice (Oryza sativa L.) for yield is of great importance for ensuring food security of the population. Living organisms manifest genetically determined responses to environmental factors, including stressors. Photosynthetic activity affects all metabolic processes in plant cells. The genes involved in photosynthesis, in their turn, are regulated by differentially expressed genes associated with circadian rhythms. Plants, as sedentary organisms, require more efficient regulation of gene expression. GATA factors are transcription factors (TFs) that affect the production of phytohormones and mediate the stress response. GATA factors are divided into four main classes (A to D), based on the difference in the structure of the zinc finger domain, and into seven subfamilies, depending on the availability of additional domains. GATA TFs incorporate domain structures that may be involved in the regulation of circadian rhythms. Effects on the circadian rhythms influence other regulatory metabolic pathways in plants, which makes the study of genes associated with circadian rhythms relevant and significant. The most well-known and popular method of gene editing at the moment is the CRISPR/Cas technology. More than 30 rice genes were successfully genomically edited using the CRISPR/Cas technology in the period from 2018 through 2023. This helped to improve their valuable agronomic traits.

This review summarizes all information about the classification and known functions of OsGATA genes and OsGATA TFs and provides evidence for the possibility of influencing the regulation of rice photoperiodicity by editing these genes.

1. Alam M.S., Kong J., Tao R., Ahmed T., Alamin M., Alotaibi S.S. et al. CRISPR/Cas9 mediated knockout of the OsbHLH024 transcription factor improves salt stress resistance in rice (Oryza sativa L.). Plants (Basel). 2022;11(9):1184. DOI: 10.3390/plants11091184

2. Behringer C., Bastakis E., Ranftl Q.L., Mayer K.F., Schwechheimer C. Functional diversification within the family of B-GATA transcription factors through the leucine-leucinemethionine domain. Plant Physiology. 2014;166(1):293-305. DOI: 10.1104/pp.114.246660

3. Behringer C., Schwechheimer C. B-GATA transcription factors – insights into their structure, regulation, and role in plant development. Frontiers in Plant Science. 2015;6:90. DOI: 10.3389/fpls.2015.00090

4. Biswal A.K., Mangrauthia S.K., Reddy M.R., Yugandhar P. CRISPR mediated genome engineering to develop climate smart rice: Challenges and opportunities. Seminars in Cell and Developmental Biology. 2019;96:100-106. DOI: 10.1016/j.semcdb.2019.04.005

5. Caddell D., Langenfeld N.J., Eckels M.J., Zhen S., Klaras R., Mishra L. et al. Photosynthesis in rice is increased by CRISPR/Cas9-mediated transformation of two truncated light-harvesting antenna. Frontiers in Plant Science. 2023;14:1050483. DOI: 10.3389/fpls.2023.1050483

6. Chandra D., Cho K., Pham H.A., Lee J.Y., Han O. Down-regulation of rice glutelin by CRISPR-Cas9 gene editing decreases carbohydrate content and grain weight and modulates synthesis of seed storage proteins during seed maturation. International Journal of Molecular Sciences. 2023;24(23):16941. DOI: 10.3390/ijms242316941

7. Charpentier E., Richter H., van der Oost J., White M.F. Biogenesis pathways of RNA guides in archaeal and bacterial CRISPR-Cas adaptive immunity. FEMS Microbiology Reviews. 2015;39(3):428-441. DOI: 10.1093/femsre/fuv023

8. Dong S., Dong X., Han X., Zhang F., Zhu Y., Xin X. et al. OsPDCD5 negatively regulates plant architecture and grain yield in rice. Proceedings of the National Academy of Sciences of the United States of America. 2021;118(29):e2018799118. DOI: 10.1073/pnas.2018799118

9. Duy P.N., Lan D.T., Thu H.P., Thu H.P.T., Thanh H.N., Pham N.P. et al. Improved bacterial leaf blight disease resistance in the major elite Vietnamese rice cultivar TBR225 via editing of the OsSWEET14 promoter. PLoS One. 2021;16(9):e0255470. DOI: 10.1371/journal.pone.0255470

10. Fan X., Wang P., Qi F., Hu Y., Li S., Zhang J. et al. The CCT transcriptional activator Ghd2 constantly delays the heading date by upregulating CO in rice. Journal of Genetics and Genomics. 2023;50(10):755-764. DOI: 10.1016/j.jgg.2023.03.002

11. Federal State Statistics Service: [website]. [in Russian] (Федеральная служба государственной статистики: [сайт]). URL: http://rosstat.gov.ru/shmp/2021 [дата обращения: 03.10.2024].

12. Feng Y., Zhao Y., Ma Y., Liu D., Shi H. Single-cell transcriptome analyses reveal cellular and molecular responses to low nitrogen in burley tobacco leaves. Physiologia Plantarum. Feng Z., Zhang B., Ding W., Liu X., Yang D.L., Wei P. et al. Efficient genome editing in plants using a CRISPR/Cas system. Cell Research. 2013;23(10):1229-1232. DOI: 10.1038/cr.2013.114

13. Fu S., Wang K., Ma T., Liang Y., Ma Z., Wu J. et al. An evolutionarily conserved C4HC3-type E3 ligase regulates plant broad-spectrum resistance against pathogens. The Plant Cell. 2022;34(5):1822-1843. DOI: 10.1093/plcell/koac055

14. Guo M., Chen H., Dong S., Zhang Z., Luo H. CRISPR-Cas gene editing technology and its application prospect in medicinal plants. Chinese Medicine. 2022;17(1):33. DOI: 10.1186/s13020-022-00584-w

15. Gupta P., Nutan K.K., Sinha-Pareek S.L., Pareek A. Abiotic stresses cause differential regulation of alternative splice forms of GATA transcription factor in rice. Frontiers in Plant Science. 2017;8:1944. DOI: 10.3389/fpls.2017.01944

16. He L., Li P., Xiang X., Li J., Zhang K. Some photosynthetic characteristics in transgenic rice with maize phosphoenolpyruvate carboxylase gene (pepc). Plant Physiology Communications. 2005;41:461-463. water saving technologies. Theoretical and Applied Genetics. 2022;135(1):17-33. DOI: 10.1007/s00122-021-03899-8

17. Honma Y., Adhikari P.B., Kuwata K., Kagenishi T., Yokawa K., Notaguchi M. et al. High-quality sugar production by osgcs1 rice. Communication Biology. 2020;3(1):617. DOI: 10.1038/s42003-020-01329-x

18. Huang Q., Lin B., Cao Y., Zhang Y., Song H., Huang C. et al. CRISPR/Cas9-mediated mutagenesis of the susceptibility gene OsHPP04 in rice confers enhanced resistance to rice root-knot nematode. Frontiers in Plant Science. 2023;14:1134653. DOI: 10.3389/fpls.2023.1134653

19. Hudson D., Guevara D.R., Hand A.J., Xu Z., Hao L., Chen X. et al. Rice cytokinin GATA transcription Factor1 regulates chloroplast development and plant architecture. Plant Physiology. 2013;162(1):132-144. DOI: 10.1104/pp.113.217265

20. International Rice Genome Sequencing Project, Sasaki T. The map-based sequence of the rice genome. Nature. 2005;436(7052):793-800. DOI: 10.1038/nature03895

21. Ishino Y., Shinagawa H., Makino K., Amemura M., Nakata A. Nucleotide sequence of the iap gene, responsible for alkaline phosphatase isozyme conversion in Escherichia coli, and identification of the gene product. Journal of Bacteriology. 1987;169(12):5429-5433. DOI: 10.1128/jb.169.12.5429-5433.1987

22. Itoh J.I., Nonomura K.I., Ikeda K., Yamaki S., Inukai Y., Yamagishi H. et al. Rice plant development: from zygote to spikelet. Plant and Cell Physiology. 2005;46(1):23-47. DOI: 10.1093/pcp/pci501

23. Izawa T. Daylength measurements by rice plants in photoperiodic short-day flowering. International Review of Cytology. 2007;256:191-222. DOI: 10.1016/S0074-7696(07)56006-7

24. Jiang W., Zhou H., Bi H., Fromm M., Yang B., Weeks D.P. Demonstration of CRISPR/Cas9/sgRNA-mediated targeted gene modification in Arabidopsis, tobacco, sorghum and rice. Nucleic Acids Research. 2013;41(20):e188. DOI: 10.1093/nar/gkt780

25. Jin J., Gui S., Li Q., Wang Y., Zhang H., Zhu Z. et al. The transcription factor GATA10 regulates fertility conversion of a two-line hybrid tms5 mutant rice via the modulation of Ub expression. Journal of Integrative Plant Biology.

26. He P., Wang X., Zhang X., Jiang Y., Tian W., Zhang X. et al. Short and narrow flag leaf1, a GATA zinc finger domain-containing protein, regulates flag leaf size in rice (Oryza sativa). BMC Plant Biology. 2018;18(1):273. DOI: 10.1186/s12870-018-1452-9

27. Heredia M.C., Kant J., Prodhan M.A., Dixit S., Wissuwa M. Breeding rice for a changing climate by improving adaptations to 2020;62(7):1034-1056. DOI: 10.1111/jipb.12871

28. Jinek M., Chylinski K., Fonfara I., Hauer M., Doudna J.A., Charpentier E. A programmable dual-RNA-guided DNA endonuclease in adaptive bacterial immunity. Science (New York, N.Y.). 2012;337(6096):816-821. DOI: 10.1126/science.1225829

29. Khandagale K.S., Chavhan R., Nadaf A.B. RNAi-mediated down regulation of BADH2 gene for expression of 2-acetyl-1-pyrroline in non-scented indica rice IR-64 (Oryza sativa L.). 3 Biotech. 2020;10(4):145. DOI: 10.1007/s13205-020-2131-8

30. Lee J.H., Won H.J., Tran P.H.N., Lee S.M, Kim H.Y., Jung J.H. Improving lignocellulosic biofuel production by CRISPR/ Cas9-mediated lignin modification in barley. GCB Bioenergy. 2021;13(4):742-752. DOI: 10.1111/gcbb.12808

31. Li B., Cui G., Shen G., Zhan Z., Huang L., Chen J. et al. Targeted mutagenesis in the medicinal plant Salvia miltiorrhiza. Scientific Reports. 2017;7:43320. DOI: 10.1038/srep43320

32. Li Y., Lu Y.F., Zhou Y., Wei X., Peng Y., Dai Y. et al. Diurnal transcriptomics analysis reveals the regulatory role of the circadian rhythm in super-hybrid rice LY2186. Genomics. 2021;113(3):1281-1290. DOI: 10.1016/j.ygeno.2020.12.046

33. Lim C., Kim Y., Shim Y., Cho S.H., Yang T.J., Song Y.H. et al. Rice OsGATA16 is a positive regulator for chlorophyll biosynthesis and chloroplast development. The Plant Journal: for Cell and Molecular Biology. 2024;117(2):599-615. DOI: 10.1111/tpj.16517

34. Lisch D.R., Freeling M., Langham R.J., Choy M.Y. Mutator transposase is widespread in the grasses. Plant Physiology. 2001;125(3):1293-1303. DOI: 10.1104/pp.125.3.1293

35. Liu M., Rehman S., Tang X., Gu K., Fan Q., Chen D. et al. Methodologies for improving HDR efficiency. Frontiers in Genetics. 2019;9:691. DOI: 10.3389/fgene.2018.00691

36. Liu Q., Yang F., Zhang J., Liu H., Rahman S., Islam S. et al. Application of CRISPR/Cas9 in crop quality improvement. International Journal of Molecular Sciences. 2021;22(8):4206. DOI: 10.3390/ijms22084206

37. Lu G., Casaretto J.A., Ying S., Mahmood K., Liu F., Bi Y.M. et al. Overexpression of OsGATA12 regulates chlorophyll content, delays plant senescence and improves rice yield under high density planting. Plant Molecular Biology. 2017;94(1-2):215-227. DOI: 10.1007/s11103-017-0604-x

38. Matsumoto T., Wu J., Itoh T., Numa H., Antonio B., Sasaki T. The Nipponbare genome and the next-generation of rice genomics research in Japan. Rice (New York, N.Y.). 2016;9(1):33. DOI: 10.1186/s12284-016-0107-4

39. McWatters H.G., Roden L.C., Staiger D. Picking out parallels: plant circadian clocks in context. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences. 2001;356(1415):1735-1743. DOI: 10.1098/rstb.2001.0936

40. Miao C., Xiao L., Hua K., Zou C., Zhao Y., Bressan R.A. et al. Mutations in a subfamily of abscisic acid receptor genes promote rice growth and productivity. Proceedings of the National Academy of Sciences of the United States of America. 2018;115(23):6058-6063. DOI: 10.1073/pnas.1804774115

41. Miao J., Guo D., Zhang J., Huang Q., Qin G., Zhang X. et al. Targeted mutagenesis in rice using CRISPR-Cas system. Cell Research. 2013;23(10):1233-1236. DOI: 10.1038/cr.2013.123

42. NCBI. National Center for Biotechnology Information: [website]. Available from: https://www.ncbi.nlm.nih.gov [accessed Apr. 15, 2024].

43. Nurhayati, Ardie S.W., Santoso T.J., Sudarsono. CRISPR/Cas9mediated genome editing in rice cv. IPB3S results in a semi-dwarf phenotypic mutant. Biodiversitas Journal of Biological Diversity. 2021;22(9):3792-3800. DOI: 10.13057/biodiv/d220924

44. Nutan K.K., Singla-Pareek S.L., Pareek A. The Saltol QTL-localized transcription factor OsGATA8 plays an important role in stress tolerance and seed development in Arabidopsis and rice. Journal of Experimental Botany. 2020;71(2):684-698. DOI: 10.1093/jxb/erz368

45. Oryzabase, sponsored by NBRP. Integrated Rice Science Database: [website]. Available from: https://shigen.nig.ac.jp/ rice/oryzabase/ [accessed Apr. 15, 2024].

46. Paajanen P., de Barros Dantas L.L., Dodd A.N. Layers of crosstalk between circadian regulation and environmental signalling in plants. Current Biology. 2021;31(8):R399-R413. DOI: 10.1016/j.cub.2021.03.046

47. Phytozome 13. The Plant Genomics Resource: [website]. Available from: https://phytozome-next.jgi.doe.gov/ [accessed Apr. 15, 2024].

48. Rao Y., Li Y., Qian Q. Recent progress on molecular breeding of rice in China. Plant Cell Reports. 2014;33(4):551-564. DOI: 10.1007/s00299-013-1551-x

49. RAP-DB. The Rice Annotation Project Database: [website]. Available from: https://rapdb.dna.affrc.go.jp/ [accessed Apr. 15, 2024].

50. Reyes J.C., Muro-Pastor M.I., Florencio F.J. The GATA family of transcription factors in Arabidopsis and rice. Plant Physiology. 2004;134(4):1718-1732. DOI: 10.1104/pp.103.037788

51. Richter R., Behringer C., Müller I.K., Schwechheimer C. The GATA-type transcription factors GNC and GNL/CGA1 repress gibberellin signaling downstream from DELLA proteins and PHYTOCHROME-INTERACTING FACTORS. Genes and Development. 2010;24(18):2093-2104. DOI: 10.1101/gad.594910

52. Schwechheimer C., Schröder P.M., Blaby-Haas C.E. Plant GATA factors: their biology, phylogeny, and phylogenomics. Annual Review of Plant Biology. 2022;73:123-148. DOI: 10.1146/annurev-arplant-072221-092913

53. Shan Q., Wang Y., Li J., Zhang Y., Chen K., Liang Z. et al. Targeted genome modification of crop plants using a CRISPRCas system. Nature Biotechnology. 2013;31(8):686-688. DOI: 10.1038/nbt.2650

54. Shen G., Hu W., Zhang B., Xing Y. The regulatory network mediated by circadian clock genes is related to heterosis in rice. Journal of Integrative Plant Biology. 2015;57(3):300-312. DOI: 10.1111/jipb.12240

55. Sheng X., Ai Z., Tan Y., Hu Y., Guo X., Liu X. et al. Novel salinitytolerant third-generation hybrid rice developed via CRISPR/Cas9-mediated gene editing. International Journal of Molecular Sciences. 2023;24(9):8025. DOI: 10.3390/ijms24098025

56. Sun C., He C., Zhong C., Liu S., Liu H., Luo X. et al. Bifunctional regulators of photoperiodic flowering in short day plant rice. Frontiers in Plant Science. 2022;13:1044790. DOI: 10.3389/fpls.2022.1044790

57. Sun Y., Zhang X., Wu C., He Y., Ma Y., Hou H. et al. Engineering herbicide-resistant rice plants through CRISPR/Cas9mediated homologous recombination of acetolactate synthase. Molecular Plant. 2016;9(4):628-631. DOI: 10.1016/j.molp.2016.01.001

58. Swinnen G., Jacobs T., Pauwels L., Goossens A. CRISPR-Casmediated gene knockout in tomato. Methods in Molecular Biology (Clifton, N.J.). 2020;2083:321-341. DOI: 10.1007/978-1-4939-9952-1_25

59. Toniutti L., Breitler J.C., Guittin C., Doulbeau S., Etienne H., Campa C. et al. An altered circadian clock coupled with a higher photosynthesis efficiency could explain the better agronomic performance of a new coffee clone when compared with a standard variety. International Journal of Molecular Sciences. 2019;20(3):736. DOI: 10.3390/ijms20030736

60. Ukhatova Y.V., Erastenkova M.V., Korshikova E.S., Krylova E.A., Mikhailova A.S., Semilet T.V. et al. Improvement of crops using the CRISPR/Cas system: new target genes. Molecular Biology. 2023;57(3):387-410. [in Russian] DOI: 10.31857/s0026898423030151

61. Usman B., Nawaz G., Zhao N., Liao S., Liu Y., Li R. Precise editing of the OsPYL9 gene by RNA-guided Cas9 nuclease confers enhanced drought tolerance and grain yield in rice (Oryza sativa L.) by regulating circadian rhythm and abiotic stress responsive proteins. International Journal of Molecular Sciences. 2020a;21(21):7854. DOI: 10.3390/ijms21217854

62. Usman B., Nawaz G., Zhao N., Liu Y., Li R. Generation of high yielding and fragrant rice (Oryza sativa L.) lines by CRISPR/Cas9 targeted mutagenesis of three homoeologs of cytochrome P450 gene family and OsBADH2 and transcriptome and proteome profiling of revealed changes triggered by mutations. Plants (Basel). 2020b;9(6):788. DOI: 10.3390/plants9060788

63. Vicentini G., Biancucci M., Mineri L., Chirivì D., Giaume F., Miao Y. et al. Environmental control of rice flowering time. Plant Communications. 2023;4(5):100610. DOI: 10.1016/j.xplc.2023.100610

64. Vorobyev N.V. Physiological bases of rice harvest formation: a monograph (Fiziologicheskiye osnovy formirovaniya urozhaya risa: monografiya). Krasnodar: All-Russian Rice Research Institute; 2013. [in Russian]

65. Wang G., Wang C., Lu G., Wang W., Mao G., Habben J.E. et al. Knockouts of a late flowering gene via CRISPR–Cas9 confer early maturity in rice at multiple field locations. Plant Molecular Biology. 2020;104(1-2):137-150. DOI: 10.1007/s11103-020-01031-w

66. Wang L., Yin H., Qian Q., Yang J., Huang C., Hu X. et al. NECK LEAF 1, a GATA type transcription factor, modulates organogenesis by regulating the expression of multiple regulatory genes during reproductive development in rice. Cell Research. 2009;19(5):598-611. DOI: 10.1038/cr.2009.36

67. Wu Q., Liu Y., Huang J. CRISPR-Cas9 mediated mutation in OsPUB43 improves grain length and weight in rice by promoting cell proliferation in spikelet hull. International Journal of Molecular Sciences. 2022;23(4):2347. DOI: 10.3390/ijms23042347

68. Wyman C., Kanaar R. DNA double-strand break repair: all’s well that ends well. Annual Review of Genetics. 2006;40:363-383. DOI: 10.1146/annurev.genet.40.110405.090451

69. Xu Y., Wang H., Lu Z., Wen L., Gu Z., Zhang X. et al. Developmental analysis of the GATA factor HANABA TARANU mutants in Medicago truncatula reveals their roles in nodule formation. Frontiers in Plant Science. 2021;12:616776. DOI: 10.3389/fpls.2021.616776

70. Yadavalli V., Neelam S., Rao A.S.V.C., Reddy A.R., Subramanyam R. Differential degradation of photosystem I subunits under iron deficiency in rice. Journal of Plant Physiology. 2012;169(8):753-759. DOI: 10.1016/j.jplph.2012.02.008

71. Yang J., Fang Y., Wu H., Zhao N., Guo X., Mackon E. et al. Improvement of resistance to rice blast and bacterial leaf streak by CRISPR/Cas9-mediated mutagenesis of Pi21 and OsSULTR3;6 in rice (Oryza sativa L.). Frontiers in Plant Science. 2023;14:1209384. DOI: 10.3389/fpls.2023.1209384

72. Yang T., Zeng R., Zhu H., Chen L., Zhang Z., Ding X. et al. Effect of grain length gene GS3 in pyramiding breeding of rice. Molecular Plant Breeding. 2010;8:59-66.

73. Yano K., Yamamoto E., Aya K., Takeuchi H., Lo P.C., Hu L. et al. Genome-wide association study using whole-genome sequencing rapidly identifies new genes influencing agronomic traits in rice. Nature Genetics. 2016;48(8):927-934. DOI: 10.1038/ng.3596

74. Ye H., Du H., Tang N., Li X., Xiong L. Identification and expression profiling analysis of TIFY family genes involved in stress and phytohormone responses in rice. Plant Molecular Biology. 2009;71(3):291-305. DOI: 10.1007/s11103-009-9524-8

75. Zegeye W.A., Chen D., Islam M.A., Wang H., Riaz A., Rani M.H. et al. OsFBK4, a novel GA insensitive gene positively regulates plant height in rice (Oryza sativa L.). Ecological Genetics and Genomics. 2022;23:100115. DOI: 10.1016/j.egg.2022.100115

76. Zeng X., Luo Y., Vu N.T.Q., Shen S., Xia K., Zhang M. CRISPR/ Cas9-mediated mutation of OsSWEET14 in rice cv. Zhonghua11 confers resistance to Xanthomonas oryzae pv. oryzae without yield penalty. BMC Plant Biology. 2020;20(1):313. DOI: 10.1186/s12870-020-02524-y

77. Zhang H., Wu T., Li Z., Huang K., Kim N.E., Ma Z. et al. OsGATA16, a GATA transcription factor, confers cold tolerance by repressing OsWRKY45–1 at the seedling stage in rice. Rice (New York, N.Y.). 2021;14(1):42. DOI: 10.1186/s12284-021-00485-w

78. Zhang J., Zeng D., Zhu Y., Xie H., Cai Q., Lian L. et al. Breeding of rice restore lines with white-backed planthopper resistance by marker-assisted selection. Chinese Journal of Rice Science. 2013;27(3):329-334.

79. Zhang Y., Chen G., Deng L., Gao B., Yang J., Ding C. et al. Integrated 3D genome, epigenome and transcriptome analyses reveal transcriptional coordination of circadian rhythm in rice. Nucleic Acids Research. 2023;51(17):9001-9018. DOI: 10.1093/nar/gkad658

80. Zhang Y.J., Zhang Y., Zhang L.L., He J.X., Xue H.W., Wang J.W. et al. The transcription factor OsGATA6 regulates rice heading date and grain number per panicle. Journal of Experimental Botany. 2022;73(18):6133-6149. DOI: 10.1093/jxb/erac247

81. Zhang Y.J., Zhang Y., Zhang L.L., Huang H.Y., Yang B.J., Luan S. et al. OsGATA7 modulates brassinosteroids-mediated growth regulation and influences architecture and grain shape. Plant Biotechnology Journal. 2018;16(7):1261-1264. DOI: 10.1111/pbi.12887

82. Zhao Y., Medrano L., Ohashi K., Fletcher J.C., Yu H., Sakai H. et al. HANABA TARANU is a GATA transcription factor that regulates shoot apical meristem and flower development in Arabidopsis. The Plant Cell. 2004;16(10):2586-2600. DOI: 10.1105/tpc.104.024869

83. Zheng S., Ye C., Lu J., Liufu J., Lin L., Dong Z. et al. Improving the rice photosynthetic efficiency and yield by editing OsHXK1 via CRISPR/Cas9 system. International Journal of Molecular Sciences. 2021;22(17):9554. DOI: 10.3390/ijms22179554

84. Zheng Y., Sun Y., Liu Y. Emerging roles of FHY3 and FAR1 as system integrators in plant development. Plant and Cell Physiology. 2023;64(10):1139-1145. DOI: 10.1093/pcp/pcad068

85. Zong G., Wang A., Wang L., Liang G., Gu M., Sang T. et al. A pyramid breeding of eight grain-yield related quantitative trait loci based on marker-assistant and phenotype selection in rice (Oryza sativa L.). Journal of Genetics and Genomics. 2012;39(7):335-350. DOI: 10.1016/j.jgg.2012.06.004