Initiation of scutellum-derived callus is regulated by an embryo-like developmental pathway in rice.

Fu Guo, Hua Wang, Guiwei Lian, Gui Cai, Wu Liu, Haidao Zhang, Dandan Li, Chun Zhou, Ning Han, Muyuan Zhu, Yinghua Su, Pil Joon Seo, Lin Xu, Hongwu Bian
Author Information
  1. Fu Guo: Institute of Genetic and Regenerative Biology, Key Laboratory for Cell and Gene Engineering of Zhejiang Province, College of Life Sciences, Zhejiang University, Hangzhou, 310058, China.
  2. Hua Wang: National Key Laboratory of Plant Molecular Genetics, CAS Center for Excellence in Molecular Plant Sciences, Institute of Plant Physiology and Ecology, Chinese Academy of Sciences, 300 Fenglin Road, Shanghai, 200032, China.
  3. Guiwei Lian: Institute of Genetic and Regenerative Biology, Key Laboratory for Cell and Gene Engineering of Zhejiang Province, College of Life Sciences, Zhejiang University, Hangzhou, 310058, China.
  4. Gui Cai: National Key Laboratory of Plant Molecular Genetics, CAS Center for Excellence in Molecular Plant Sciences, Institute of Plant Physiology and Ecology, Chinese Academy of Sciences, 300 Fenglin Road, Shanghai, 200032, China.
  5. Wu Liu: National Key Laboratory of Plant Molecular Genetics, CAS Center for Excellence in Molecular Plant Sciences, Institute of Plant Physiology and Ecology, Chinese Academy of Sciences, 300 Fenglin Road, Shanghai, 200032, China.
  6. Haidao Zhang: Institute of Genetic and Regenerative Biology, Key Laboratory for Cell and Gene Engineering of Zhejiang Province, College of Life Sciences, Zhejiang University, Hangzhou, 310058, China.
  7. Dandan Li: Hainan Institute, Zhejiang University, Yazhou Bay Science and Technology City, Sanya, 572025, China.
  8. Chun Zhou: Institute of Genetic and Regenerative Biology, Key Laboratory for Cell and Gene Engineering of Zhejiang Province, College of Life Sciences, Zhejiang University, Hangzhou, 310058, China.
  9. Ning Han: Institute of Genetic and Regenerative Biology, Key Laboratory for Cell and Gene Engineering of Zhejiang Province, College of Life Sciences, Zhejiang University, Hangzhou, 310058, China.
  10. Muyuan Zhu: Institute of Genetic and Regenerative Biology, Key Laboratory for Cell and Gene Engineering of Zhejiang Province, College of Life Sciences, Zhejiang University, Hangzhou, 310058, China.
  11. Yinghua Su: State Key Laboratory of Crop Biology, Shandong Key Laboratory of Crop Biology, College of Life Sciences, Shandong Agricultural University, Taian, Shandong, 271018, China.
  12. Pil Joon Seo: Department of Chemistry, Seoul National University, Seoul, 08826, Korea. ORCID
  13. Lin Xu: National Key Laboratory of Plant Molecular Genetics, CAS Center for Excellence in Molecular Plant Sciences, Institute of Plant Physiology and Ecology, Chinese Academy of Sciences, 300 Fenglin Road, Shanghai, 200032, China. xulin@cemps.ac.cn. ORCID
  14. Hongwu Bian: Institute of Genetic and Regenerative Biology, Key Laboratory for Cell and Gene Engineering of Zhejiang Province, College of Life Sciences, Zhejiang University, Hangzhou, 310058, China. hwbian@zju.edu.cn. ORCID

Abstract

In rice (Oryza sativa) tissue culture, callus can be induced from the scutellum in embryo or from the vasculature of non-embryonic organs such as leaves, nodes, or roots. Here we show that the auxin signaling pathway triggers cell division in the epidermis of the scutellum to form an embryo-like structure, which leads to callus formation. Our transcriptome data show that embryo-, stem cell-, and auxin-related genes are upregulated during scutellum-derived callus initiation. Among those genes, the embryo-specific gene OsLEC1 is activated by auxin and involved in scutellum-derived callus initiation. However, OsLEC1 is not required for vasculature-derived callus initiation from roots. In addition, OsIAA11 and OsCRL1, which are involved in root development, are required for vasculature-derived callus formation but not for scutellum-derived callus formation. Overall, our data indicate that scutellum-derived callus initiation is regulated by an embryo-like development program, and this is different from vasculature-derived callus initiation which borrows a root development program.

References

  1. Plant Cell. 2005 May;17(5):1387-96 [PMID: 15829602]
  2. Proc Natl Acad Sci U S A. 2008 Feb 26;105(8):3151-6 [PMID: 18287041]
  3. Plant Physiol. 2017 Nov;175(3):1158-1174 [PMID: 28904073]
  4. Genome Biol. 2014;15(12):550 [PMID: 25516281]
  5. Plant Physiol. 2013 Apr;161(4):2113-27 [PMID: 23457229]
  6. Planta. 2002 Apr;214(6):829-36 [PMID: 11941458]
  7. Bioinformatics. 2010 Jan 1;26(1):139-40 [PMID: 19910308]
  8. Theor Appl Genet. 1986 Apr;72(1):3-10 [PMID: 24247763]
  9. PLoS Genet. 2012 Aug;8(8):e1002911 [PMID: 22927830]
  10. PLoS Genet. 2009 Aug;5(8):e1000605 [PMID: 19680533]
  11. Proc Natl Acad Sci U S A. 2006 Feb 28;103(9):3468-73 [PMID: 16492731]
  12. Plant Cell Physiol. 2005 Mar;46(3):399-406 [PMID: 15695450]
  13. Curr Top Dev Biol. 2014;108:1-33 [PMID: 24512704]
  14. Plant J. 2005 Jul;43(1):47-56 [PMID: 15960615]
  15. Regeneration (Oxf). 2017 Aug 27;4(3):132-139 [PMID: 28975033]
  16. Plant Cell Physiol. 2020 Sep 1;61(9):1646-1660 [PMID: 32592489]
  17. Plant Physiol. 2017 Oct;175(2):848-857 [PMID: 28830937]
  18. Curr Biol. 2015 Apr 20;25(8):1017-30 [PMID: 25819565]
  19. Nat Biotechnol. 2019 Aug;37(8):907-915 [PMID: 31375807]
  20. Bioinformatics. 2018 Sep 1;34(17):i884-i890 [PMID: 30423086]
  21. Sci Rep. 2016 Mar 14;6:23050 [PMID: 26973288]
  22. Plant Cell. 2009 Sep;21(9):2563-77 [PMID: 19767455]
  23. Plant Cell Physiol. 2018 Apr 1;59(4):734-743 [PMID: 29361138]
  24. Annu Rev Plant Biol. 2019 Apr 29;70:377-406 [PMID: 30786238]
  25. Development. 2023 Mar 1;150(5): [PMID: 36762604]
  26. Trends Cell Biol. 2011 Apr;21(4):212-8 [PMID: 21236679]
  27. Plant J. 1998 Sep;15(6):755-64 [PMID: 9807814]
  28. Bioinformatics. 2010 May 1;26(9):1273-5 [PMID: 20223836]
  29. Plant J. 2009 Aug;59(3):448-60 [PMID: 19453451]
  30. Mol Plant. 2012 Jan;5(1):154-61 [PMID: 21914651]
  31. Plants (Basel). 2021 Jul 17;10(7): [PMID: 34371670]
  32. Protoplasma. 2014 May;251(3):545-54 [PMID: 24085343]
  33. Plant Cell. 2014 Mar;26(3):1081-93 [PMID: 24642937]
  34. Planta. 2005 Dec;222(6):977-88 [PMID: 16034595]
  35. Nat Biotechnol. 2015 Mar;33(3):290-5 [PMID: 25690850]
  36. Front Genet. 2020 Jul 17;11:766 [PMID: 32765593]
  37. Nature. 2007 Apr 12;446(7137):811-4 [PMID: 17429400]
  38. EMBO J. 2018 Oct 15;37(20): [PMID: 30061313]
  39. Plant Cell Rep. 2017 Jun;36(6):843-858 [PMID: 28255787]
  40. Plant Cell. 2004 May;16(5):1206-19 [PMID: 15084721]
  41. Plant J. 2002 May;30(3):349-59 [PMID: 12000682]
  42. Plant J. 2009 Feb;57(4):626-44 [PMID: 18980654]
  43. Plant Cell Environ. 2016 Oct;39(10):2288-302 [PMID: 27342100]
  44. Dev Cell. 2010 Mar 16;18(3):463-71 [PMID: 20230752]
  45. PLoS One. 2012;7(1):e30039 [PMID: 22253868]
  46. Dev Cell. 2020 Sep 28;54(6):742-757.e8 [PMID: 32755547]
  47. Front Plant Sci. 2022 May 10;13:887980 [PMID: 35620685]
  48. Plant Cell Physiol. 2018 Sep 1;59(9):1782-1789 [PMID: 29788450]
  49. Planta. 2007 Oct;226(5):1183-94 [PMID: 17581762]
  50. Plant Physiol. 2003 Oct;133(2):653-63 [PMID: 14512519]
  51. Proc Natl Acad Sci U S A. 2016 May 3;113(18):5101-6 [PMID: 27092001]
  52. BMC Bioinformatics. 2008 Dec 29;9:559 [PMID: 19114008]
  53. Dev Cell. 2004 Sep;7(3):373-85 [PMID: 15363412]
  54. Genome Res. 2017 Mar;27(3):491-499 [PMID: 28100584]
  55. Nat Methods. 2015 Apr;12(4):357-60 [PMID: 25751142]
  56. Plant Cell. 2013 Sep;25(9):3159-73 [PMID: 24076977]
  57. Plant Physiol. 2004 Nov;136(3):3660-9 [PMID: 15516508]
  58. Plant Mol Biol. 2010 Jul;73(4-5):481-92 [PMID: 20405311]
  59. Plant Cell. 2002 Aug;14(8):1737-49 [PMID: 12172019]
  60. Nat Plants. 2021 Nov;7(11):1453-1460 [PMID: 34782770]
  61. Proc Natl Acad Sci U S A. 2001 Sep 25;98(20):11806-11 [PMID: 11573014]
  62. Plant Cell Environ. 2021 Sep;44(9):3103-3121 [PMID: 33993496]
  63. Cell. 1998 Jun 26;93(7):1195-205 [PMID: 9657152]
  64. Curr Biol. 2011 Mar 22;21(6):508-14 [PMID: 21396822]
  65. Plant Cell. 2003 Jan;15(1):5-18 [PMID: 12509518]
  66. New Phytol. 2012 Oct;196(1):149-161 [PMID: 22846038]
  67. Proc Natl Acad Sci U S A. 2015 Mar 17;112(11):3570-5 [PMID: 25733849]
  68. Cell Res. 2012 Jul;22(7):1169-80 [PMID: 22508267]
  69. Nucleic Acids Res. 2017 Jan 4;45(D1):D1040-D1045 [PMID: 27924042]
  70. Sci Rep. 2020 Dec 4;10(1):21257 [PMID: 33277567]
  71. New Phytol. 2021 Mar;229(5):2676-2692 [PMID: 33135782]

MeSH Term

Oryza
Plant Roots
Indoleacetic Acids
Signal Transduction

Chemicals

Indoleacetic Acids