Auxin apical dominance governed by the OsAsp1-OsTIF1 complex determines distinctive rice caryopses development on different branches

English version

Autoři: Shu Chang ^aff001; Yixing Chen ^aff001; Shenghua Jia ^aff001; Yihao Li ^aff001; Kun Liu ^aff001; Zhouhua Lin ^aff001; Hanmeng Wang ^aff001; Zhilin Chu ^aff001; Jin Liu ^aff001; Chao Xi ^aff001; Heping Zhao ^aff001; Shengcheng Han ^aff001; Yingdian Wang ^aff001
Působiště autorů: Beijing Key Laboratory of Gene Resource and Molecular Development, College of Life Sciences, Beijing Normal University, China ^aff001; Academy of Plateau Science and Sustainability of the People's Government of Qinghai Province & Beijing Normal University, Qinghai Normal University, Qinghai, China ^aff002
Vyšlo v časopise: Auxin apical dominance governed by the OsAsp1-OsTIF1 complex determines distinctive rice caryopses development on different branches. PLoS Genet 16(10): e1009157. doi:10.1371/journal.pgen.1009157
Kategorie: Research Article
doi: https://doi.org/10.1371/journal.pgen.1009157

Souhrn

In rice (Oryza sativa), caryopses located on proximal secondary branches (CSBs) have smaller grain size and poorer grain filling than those located on apical primary branches (CPBs), greatly limiting grain yield. However, the molecular mechanism responsible for developmental differences between CPBs and CSBs remains elusive. In this transcriptome-wide expression study, we identified the gene Aspartic Protease 1 (OsAsp1), which reaches an earlier and higher transcriptional peak in CPBs than in CSBs after pollination. Disruption of OsAsp1 expression in the heterozygous T-DNA line asp1-1^+/–eliminated developmental differences between CPBs and CSBs. OsAsp1 negatively regulated the transcriptional inhibitor of auxin biosynthesis, OsTAA1 transcriptional inhibition factor 1 (OsTIF1), to preserve indole-3-acetic acid (IAA) apical dominance in CPBs and CSBs. IAA also facilitated OsTIF1 translocation from the endoplasmic reticulum (ER) to the nucleus by releasing the interaction of OsTIF1 with OsAsp1 to regulate caryopses IAA levels via a feedback loop. IAA promoted transcription of OsAsp1 through MADS29 to maintain an OsAsp1 differential between CPBs and CSBs during pollination. Together, these findings provide a mechanistic explanation for the distributed auxin differential between CPBs and CSBs to regulate distinct caryopses development in different rice branches and potential targets for engineering yield improvement in crops.

Klíčová slova:

Arabidopsis thaliana – Auxins – Endoplasmic reticulum – Endosperm – Gene expression – Mesophyll – Rice – Transcriptional control

Zdroje

1. Xing Y, Zhang Q. Genetic and molecular bases of rice yield. Annual Review of Plant Biology. 2010;61(1):421–42. doi: 10.1146/annurev-arplant-042809-112209 20192739

2. Yang J, Zhang J. Grain-filling problem in ‘super’ rice. Journal of Experimental Botany. 2010;61(1):1–5. doi: 10.1093/jxb/erp348 19959608

3. Song XJ, Kuroha T, Ayano M, Furuta T, Nagai K, Komeda N, et al. Rare allele of a previously unidentified histone H4 acetyltransferase enhances grain weight, yield, and plant biomass in rice. Proceedings of the National Academy of Sciences. 2015;112(1):76–81. doi: 10.1073/pnas.1421127112 25535376

4. Song X-J, Huang W, Shi M, Zhu M-Z, Lin H-X. A QTL for rice grain width and weight encodes a previously unknown RING-type E3 ubiquitin ligase. Nature Genetics. 2007;39 : 623. doi: 10.1038/ng2014 17417637

5. Shomura A, Izawa T, Ebana K, Ebitani T, Kanegae H, Konishi S, et al. Deletion in a gene associated with grain size increased yields during rice domestication. Nature Genetics. 2008;40 : 1023. doi: 10.1038/ng.169 18604208

6. Weng J, Gu S, Wan X, Gao H, Guo T, Su N, et al. Isolation and initial characterization of GW5, a major QTL associated with rice grain width and weight. Cell Research. 2008;18 : 1199. doi: 10.1038/cr.2008.307 19015668

7. Miao J, Yang Z, Zhang D, Wang Y, Xu M, Zhou L, et al. Mutation of RGG2, which encodes a type B heterotrimeric G protein γ subunit, increases grain size and yield production in rice. Plant Biotechnology Journal. 2018. doi: 10.1111/pbi.13005 30160362

8. Sun S, Wang L, Mao H, Shao L, Li X, Xiao J, et al. A G-protein pathway determines grain size in rice. Nature Communications. 2018;9(1):851. doi: 10.1038/s41467-018-03141-y 29487318

9. Xu R, Duan P, Yu H, Zhou Z, Zhang B, Wang R, et al. Control of grain size and weight by the OsMKKK10-OsMKK4-OsMAPK6 signaling pathway in rice. Molecular Plant. 2018;11(6):860–73. doi: 10.1016/j.molp.2018.04.004 29702261

10. Li Y, Fan C, Xing Y, Jiang Y, Luo L, Sun L, et al. Natural variation in GS5 plays an important role in regulating grain size and yield in rice. Nature Genetics. 2011;43 : 1266. doi: 10.1038/ng.977 22019783

11. Qi P, Lin Y-S, Song X-J, Shen J-B, Huang W, Shan J-X, et al. The novel quantitative trait locus GL3.1 controls rice grain size and yield by regulating Cyclin-T1;3. Cell Research. 2012;22 : 1666. doi: 10.1038/cr.2012.151 23147796

12. Zhang X, Wang J, Huang J, Lan H, Wang C, Yin C, et al. Rare allele of OsPPKL1 associated with grain length causes extra-large grain and a significant yield increase in rice. Proceedings of the National Academy of Sciences. 2012;109(52):21534–9. doi: 10.1073/pnas.1219776110 23236132

13. Ishimaru K, Hirotsu N, Madoka Y, Murakami N, Hara N, Onodera H, et al. Loss of function of the IAA-glucose hydrolase gene TGW6 enhances rice grain weight and increases yield. Nature Genetics. 2013;45(6):707–11. doi: 10.1038/ng.2612 23583977

14. Liu L, Tong H, Xiao Y, Che R, Xu F, Hu B, et al. Activation of Big Grain1 significantly improves grain size by regulating auxin transport in rice. Proceedings of the National Academy of Sciences. 2015;112(35):11102–7. doi: 10.1073/pnas.1512748112 26283354

15. Kato T, Shinmura D, Taniguchi A. Activities of enzymes for sucrose–starch conversion in developing endosperm of rice and their association with grain filling in extra-heavy panicle types. Plant Production Science. 2007;10(4):442–50. doi: 10.1626/pps.10.442

16. Xu G, Zhang J, Lam HM, Wang Z, Yang J. Hormonal changes are related to the poor grain filling in the inferior spikelets of rice cultivated under non-flooded and mulched condition. Field Crops Research. 2007;101(1):53–61.

17. Yang J, Zhang J, Wang Z, Liu K, Wang P. Post-anthesis development of inferior and superior spikelets in rice in relation to abscisic acid and ethylene. Journal of Experimental Botany. 2006;57(1):149–60. doi: 10.1093/jxb/erj018 16330527

18. Zhang H, Tan G, Yang L, Yang J, Zhang J, Zhao B. Hormones in the grains and roots in relation to post-anthesis development of inferior and superior spikelets in japonica/indica hybrid rice. Plant Physiology & Biochemistry. 2009;47(3):195–204. doi: 10.1016/j.plaphy.2008.11.012 19117763

19. Chen T, Xu G, Wang Z, Zhang H, Yang J, Zhang J. Expiression of proteins in superior and inferior spikelets of rice during grain filling under different irrigation regimes. Proteomics. 2016;16(1):102–21. doi: 10.1002/pmic.201500070 26442785

20. Zhu G, Ye N, Yang J, Peng X, Zhang J. Regulation of expression of starch synthesis genes by ethylene and ABA in relation to the development of rice inferior and superior spikelets. Journal of Experimental Botany. 2011;62(11):3907–16. doi: 10.1093/jxb/err088 21459770

21. Peng T, Lv Q, Zhang J, Li J, Du Y, Zhao Q. Differential expression of the microRNAs in superior and inferior spikelets in rice (Oryza sativa). Journal of Experimental Botany. 2011;62(14):4943–54. doi: 10.1093/jxb/err205 21791435

22. Peng T, Sun H, Qiao M, Zhao Y, Du Y, Zhang J, et al. Differentially expressed microRNA cohorts in seed development may contribute to poor grain filling of inferior spikelets in rice. BMC Plant Biology. 2014;14(1):1–17. doi: 10.1186/s12870-014-0196-4 25052585

23. Ishimaru T, Matsuda T, Ohsugi R, Yamagishi T. Morphological development of rice caryopses located at the different positions in a panicle from early to middle stage of grain filling. Functional Plant Biology. 2003;30(11):1139–49. doi: 10.1071/FP03122 32689096

24. Bi X, Khush GS, Bennett J. The rice nucellin gene ortholog OsAsp1 encodes an active aspartic protease without a plant-specific insert and is strongly expressed in early embryo. Plant and Cell Physiology. 2005;46(1):87–98. doi: 10.1093/pcp/pci002 15659452

25. Guo J, Wang F, Song J, Sun W, Zhang X-S. The expression of Orysa;CycB1;1 is essential for endosperm formation and causes embryo enlargement in rice. Planta. 2010;231(2):293–303. doi: 10.1007/s00425-009-1051-y 19921249

26. Barrôco RM, Peres A, Droual A-M, De Veylder L, Nguyen LSL, De Wolf J, et al. The cyclin-dependent kinase inhibitor Orysa;KRP1 plays an important role in seed development of rice. Plant Physiology. 2006;142(3):1053–64. doi: 10.1104/pp.106.087056 17012406

27. Su’Udi M, Cha JY, Min HJ, Ermawati N, Han CD, Min GK, et al. Potential role of the rice OsCCS52A gene in endoreduplication. Planta. 2012;235(2):387–97. doi: 10.1007/s00425-011-1515-8 21927949

28. Figueiredo DD, Batista RA, Roszak PJ, Köhler C. Auxin production couples endosperm development to fertilization. Nature Plants. 2015;1(12):1–6. doi: 10.1038/NPLANTS.2015.184 27251719

29. Yoshikawa T, Ito M, Sumikura T, Nakayama A, Nishimura T, Kitano H, et al. The rice FISH BONE gene encodes a tryptophan aminotransferase, which affects pleiotropic auxin-related processes. Plant Journal. 2014;78(6):927–36. doi: 10.1111/tpj.12517 24654985

30. Yamamoto Y, Kamiya N, Morinaka Y, Matsuoka M, Sazuka T. Auxin biosynthesis by the YUCCA genes in rice. Plant Physiology. 2007;143(3):1362–71. doi: 10.1104/pp.106.091561 17220367

31. Aoki Y, Okamura Y, Tadaka S, Kinoshita K, Obayashi T. ATTED-II in 2016: A plant coexpression database towards lineage-specific coexpression. Plant and Cell Physiology. 2016;57(1):e5. doi: 10.1093/pcp/pcv165 26546318

32. Franco-Zorrilla JM, López-Vidriero I, Carrasco JL, Godoy M, Vera P, Solano R. DNA-binding specificities of plant transcription factors and their potential to define target genes. Proceedings of the National Academy of Sciences. 2014;111(6):2367–72. doi: 10.1073/pnas.1316278111 24477691

33. Cao P, Jung K-H, Choi D, Hwang D, Zhu J, Ronald PC. The Rice Oligonucleotide Array Database: An atlas of rice gene expression. Rice. 2012;5(1):17. doi: 10.1186/1939-8433-5-17 24279809

34. Yin L-L, Xue H-W. The MADS29 transcription factor regulates the degradation of the nucellus and the nucellar projection during rice seed development. Plant Cell. 2012;24(3):1049–65. doi: 10.1105/tpc.111.094854 22408076

35. Mathan J, Bhattacharya J, Ranjan A. Enhancing crop yield by optimizing plant developmental features. Development. 2016;143(18):3283–94. doi: 10.1242/dev.134072 27624833

36. Wang B, Smith SM, Li J. Genetic regulation of shoot architecture. Annual Review of Plant Biology. 2018;69(1):437–68. doi: 10.1146/annurev-arplant-042817-040422 29553800

37. Davies DR. The structure and function of the aspartic proteinases. Annual Review of Biophysics and Biophysical Chemistry. 1990;19(1):189–215. doi: 10.1146/annurev.bb.19.060190.001201 2194475

38. Rawlings ND, Barrett AJ. Families of aspartic peptidases, and those of unknown catalytic mechanism. In Methods in Enzymology: Academic Press; 1995. p. 105–20.

39. Chen J, Ouyang Y, Wang L, Xie W, Zhang Q. Aspartic proteases gene family in rice: Gene structure and expression, predicted protein features and phylogenetic relation. Gene. 2009;442(1–2):108–18. doi: 10.1016/j.gene.2009.04.021 19409457

40. Soares A, Ribeiro Carlton SM, Simões I. Atypical and nucellin-like aspartic proteases: Emerging players in plant developmental processes and stress responses. Journal of Experimental Botany. 2019;70(7):2059–76. doi: 10.1093/jxb/erz034 30715463

41. Niu N, Liang W, Yang X, Jin W, Wilson ZA, Hu J, et al. EAT1 promotes tapetal cell death by regulating aspartic proteases during male reproductive development in rice. Nature Communications. 2013;4 : 1445. http://www.nature.com/ncomms/journal/v4/n2/suppinfo/ncomms2396_S1.html. doi: 10.1038/ncomms2396 23385589

42. Woodward AW, Bartel B. Auxin: Regulation, action, and interaction. Annals of Botany. 2005;95(5):707–35. doi: 10.1093/aob/mci083 15749753

43. Leyser O. Dynamic integration of auxin transport and signalling. Current Biology. 2006;16(11):R424–R33. doi: 10.1016/j.cub.2006.05.014 16753558

44. Casanova-Sáez R, Voß U. Auxin metabolism controls developmental decisions in land plants. Trends in Plant Science. 2019;24(8):741–54. doi: 10.1016/j.tplants.2019.05.006 31230894

45. Gallavotti A, Barazesh S, Malcomber S, Hall D, Jackson D, Schmidt RJ, et al. sparse inflorescence1 encodes a monocot-specific YUCCA-like gene required for vegetative and reproductive development in maize. Proceedings of the National Academy of Sciences. 2008;105(39):15196. doi: 10.1073/pnas.0805596105 18799737

46. Mashiguchi K, Tanaka K, Sakai T, Sugawara S, Kawaide H, Natsume M, et al. The main auxin biosynthesis pathway in Arabidopsis. Proceedings of the National Academy of Sciences. 2011;108(45):18512. doi: 10.1073/pnas.1108434108 22025724

47. Phillips KA, Skirpan AL, Liu X, Christensen A, Slewinski TL, Hudson C, et al. vanishing tassel2 encodes a grass-specific tryptophan aminotransferase required for vegetative and reproductive development in maize. The Plant Cell. 2011;23(2):550–66. Epub 2011/02/18. doi: 10.1105/tpc.110.075267 21335375

48. Abu-Zaitoon YM, Bennett K, Normanly J, Nonhebel HM. A large increase in IAA during development of rice grains correlates with the expression of tryptophan aminotransferase OsTAR1 and a grain-specific YUCCA. Physiologia Plantarum. 2012;146(4):487–99. doi: 10.1111/j.1399-3054.2012.01649.x 22582989

49. Ouyang S, Zhu W, Hamilton J, Lin H, Campbell M, Childs K, et al. The TIGR Rice Genome Annotation Resource: Improvements and new features. Nucleic Acids Research. 2007;35(Suppl. 1):D883–D7. doi: 10.1093/nar/gkl976 17145706

50. Zhao Z, Zhang Y, Liu X, Zhang X, Liu S, Xiaowen YU, et al. A role for a dioxygenase in auxin metabolism and reproductive development in rice. Developmental Cell. 2013;27(1):113–22. doi: 10.1016/j.devcel.2013.09.005 24094741

51. Xu Y, Jin W, Li N, Zhang W, Liu C, Li C, et al. UBIQUITIN-SPECIFIC PROTEASE14 interacts with ULTRAVIOLET-B INSENSITIVE4 to regulate endoreduplication and cell and organ growth in Arabidopsis. Plant Cell. 2016;28(5):1200–14. doi: 10.1105/tpc.16.00007 27099260

52. Pan X, Welti R, Wang X. Quantitative analysis of major plant hormones in crude plant extracts by high-performance liquid chromatography–mass spectrometry. Nature Protocols. 2010;5(6):986–92. doi: 10.1038/nprot.2010.37 20448544

53. Sivamani E, DeLong RK, Qu R. Protamine-mediated DNA coating remarkably improves bombardment transformation efficiency in plant cells. Plant Cell Reports. 2009;28(2):213–21. doi: 10.1007/s00299-008-0636-4 19015859

54. Bowler C, Benvenuto G, PL, Molino D, Probst AV MT, et al. Chromatin techniques for plant cells. Plant Journal. 2004;39(5):776–89. doi: 10.1111/j.1365-313X.2004.02169.x 15315638

55. Cui X, Lu F, Qiu Q, Zhou B, Gu L, Zhang S, et al. REF6 recognizes a specific DNA sequence to demethylate H3K27me3 and regulate organ boundary formation in Arabidopsis. Nature Genetics. 2016;48(6):694. doi: 10.1038/ng.3556 27111035

56. Yoo S-D, Cho Y-H, Sheen J. Arabidopsis mesophyll protoplasts: A versatile cell system for transient gene expression analysis. Nature Protocols. 2007;2(7):1565–72. doi: 10.1038/nprot.2007.199 17585298

57. Wu F-H, Shen S-C, Lee L-Y, Lee S-H, Chan M-T, Lin C-S. Tape-Arabidopsis Sandwich—a simpler Arabidopsis protoplast isolation method. Plant Methods. 2009;5(1):1–10. doi: 10.1186/1746-4811-5-16 19930690

58. Bart R, Chern M, Park C-J, Bartley L, Ronald PC. A novel system for gene silencing using siRNAs in rice leaf and stem-derived protoplasts. Plant Methods. 2006;2(1):1–9. doi: 10.1186/1746-4811-2-13 16808845

59. Ding Y, Li H, Zhang X, Xie Q, Gong Z, Yang S. OST1 kinase modulates freezing tolerance by enhancing ICE1 stability in Arabidopsis. Developmental Cell. 2015;32(3):278–89. doi: 10.1016/j.devcel.2014.12.023 25669882

60. Uchiumi T, Okamoto T. Rice fruit development is associated with an increased IAA content in pollinated ovaries. Planta. 2010;232(3):579–92. doi: 10.1007/s00425-010-1197-7 20512651

61. Ulmasov T, Murfett J, Hagen G, Guilfoyle TJ. Aux/IAA proteins repress expression of reporter genes containing natural and highly active synthetic auxin response elements. Plant Cell. 1997;9(11):1963–71. doi: 10.1105/tpc.9.11.1963 9401121

62. Clough SJ, Bent AF. Floral dip: A simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant Journal. 1998;16(6):735–43. doi: 10.1046/j.1365-313x.1998.00343.x 10069079

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