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Plant function and evolutionary biology
RESEARCH ARTICLE

Ectopic expression of a R2R3 MYB transcription factor of dove tree (Davidia involucrata) aggravates seed abortion in Arabidopsis thaliana

Jian Li A B , Tian Chen A , Fengzhen Huang A B , Penghui Dai A B , Fuxiang Cao B C and Meng Li https://orcid.org/0000-0003-2454-2157 A B D
+ Author Affiliations
- Author Affiliations

A College of Life Science and Technology, Central South University of Forestry and Technology, Changsha 410004, China.

B Hunan Research Center of Engineering Technology for Utilisation of Environmental and Resources Plant, Changsha 410004, China.

C College of Horticulture and Landscape, Hunan Agricultural University, Changsha 410004, China.

D Corresponding author. Email: limeng0422@foxmail.com

Functional Plant Biology 47(5) 454-463 https://doi.org/10.1071/FP19317
Submitted: 4 November 2019  Accepted: 12 December 2019   Published: 26 March 2020

Abstract

Serious seed abortion of dove tree (Davidia involucrate Baill.) is one of the critical factors leading to the low fecundity of this species. Seed abortion is a complicated process and various factors have been verified to synergistically determine the fate of seeds. To reveal the mechanism of seed abortion in D. involucrata, we performed transcriptome analysis in normal and abortive seeds of D. involucrata. According to the transcriptome data, we noticed that most of the genes encoding a MYB transcription factor were predominantly expressed in abortive seeds. Among these, a gene named DiMYB1 was selected and its function was validated in this study. Overexpression of DiMYB1 resulted in obviously reduced viability of transgenic seeds and seedlings, and caused a significantly higher seed abortion rate. The vegetative growth of transgenic plants was hindered, resulting in an earlier flowering time. In addition, colour changes occurred in transgenic plants. Some transgenic sprouts, stems and pods appeared purple instead of green in colour. Our finding demonstrated that DiMYB1 participates in multiple plant developmental processes, especially in seed development in Arabidopsis thaliana (L.) Heynh., which indicated the similar role of this gene in D. involucrata.

Additional keywords: anthocyanin, seed development, transgenic plants, transcriptome analysis.


References

Abe M, Kaya H, Watanabe-Taneda A, Shibuta M, Yamaguchi A, Sakamoto T, Kurata T, Ausin I, Araki T, Alonso-Blanco C (2015) FE, a phloem-specific Myb-related protein, promotes flowering through transcriptional activation of FLOWERING LOCUS T and FLOWERING LOCUS T INTERACTING PROTEIN 1. The Plant Journal 83, 1059–1068.
FE, a phloem-specific Myb-related protein, promotes flowering through transcriptional activation of FLOWERING LOCUS T and FLOWERING LOCUS T INTERACTING PROTEIN 1.Crossref | GoogleScholarGoogle Scholar | 26239308PubMed |

Allan A, Hellens R, Laing W (2008) MYB transcription factors that colour our fruit. Trends in Plant Science 13, 99–102.
MYB transcription factors that colour our fruit.Crossref | GoogleScholarGoogle Scholar | 18280199PubMed |

Appelhagen I, Lu G, Huep G, Schmelzer E, Weisshaar B, Sagasser M (2011) TRANSPARENT TESTA1 interacts with R2R3–MYB factors and affects early and late steps of flavonoid biosynthesis in the endothelium of Arabidopsis thaliana seeds. The Plant Journal 67, 406–419.
TRANSPARENT TESTA1 interacts with R2R3–MYB factors and affects early and late steps of flavonoid biosynthesis in the endothelium of Arabidopsis thaliana seeds.Crossref | GoogleScholarGoogle Scholar | 21477081PubMed |

Bai X, Zhai H, Zhu Y (2011) Arabidopsis transcription factor MYBC1 mediates seed germination by ABA. Journal of Northeast Agricultural University 42, 118–124.
Arabidopsis transcription factor MYBC1 mediates seed germination by ABA.Crossref | GoogleScholarGoogle Scholar |

Berger F (2003) Endosperm: the crossroad of seed development. Current Opinion in Plant Biology 6, 42–50.
Endosperm: the crossroad of seed development.Crossref | GoogleScholarGoogle Scholar | 12495750PubMed |

Chaudhury A, Berger F (2001) Maternal control of seed development. Seminars in Cell & Developmental Biology 12, 381–386.
Maternal control of seed development.Crossref | GoogleScholarGoogle Scholar |

Dai X, Wang L (2012) Advance of physiological research on Davidia involucrata. Journal of Zhaotong University 34, 14–17.

Dai X, Xu Y, Ma Q, Xu W, Wang T, Xue Y, Chong K (2007) Overexpression of an R1R2R3 MYB gene, OsMYB3R–2, increases tolerance to freezing, drought, and salt stress in transgenic Arabidopsis. Plant Physiology 143, 1739–1751.
Overexpression of an R1R2R3 MYB gene, OsMYB3R–2, increases tolerance to freezing, drought, and salt stress in transgenic Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 17293435PubMed |

Fang W, Song Z (1975) Chinese flora supplementary information 2. Davidiaceae. Journal of Sichuan University 1, 63–67.

Frampton J (2004) ‘MYB transcription factors: their role in growth, differentiation and disease.’ (Springer: Dordrecht, the Netherlands)

Fu L, Jin J (1992) ‘China plant red data book: rare and endangered plants. Vol. 4.’ (Science Press: Beijing, China)

Gonzalez A, Zhao M, Leavitt J, Lloyd A (2008) Regulation of the anthocyanin biosynthetic pathway by the TTG1/bHLH/Myb transcriptional complex in Arabidopsis seedlings. The Plant Journal 53, 814–827.
Regulation of the anthocyanin biosynthetic pathway by the TTG1/bHLH/Myb transcriptional complex in Arabidopsis seedlings.Crossref | GoogleScholarGoogle Scholar | 18036197PubMed |

Gupta Y, Pathak A, Singh K, Mantri S, Singh S, Tuli R (2015) De novo assembly and characterization of transcriptomes of early-stage fruit from two genotypes of Annona squamosa L. with contrast in seed number. BMC Genomics 16, 86
De novo assembly and characterization of transcriptomes of early-stage fruit from two genotypes of Annona squamosa L. with contrast in seed number.Crossref | GoogleScholarGoogle Scholar | 25766098PubMed |

Han X, Yin Q, Liu J, Jiang W, Di S, Pang Y (2017) GmMYB58 and GmMYB205 are seed-specific activators for isoflavonoid biosynthesis in Glycine max. Plant Cell Reports 36, 1889–1902.
GmMYB58 and GmMYB205 are seed-specific activators for isoflavonoid biosynthesis in Glycine max.Crossref | GoogleScholarGoogle Scholar | 28905215PubMed |

Haughn G, Chaudhury A (2005) Genetic analysis of seed coat development in Arabidopsis. Trends in Plant Science 10, 472–477.
Genetic analysis of seed coat development in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 16153880PubMed |

Kim J, Hyun W, Nguyen H, Jeong C, Xiong L, Hong S, Lee H (2015) AtMyb7, a subgroup 4 R2R3 Myb, negatively regulates ABA-induced inhibition of seed germination by blocking the expression of the bZIP transcription factor ABI5. Plant, Cell & Environment 38, 559–571.
AtMyb7, a subgroup 4 R2R3 Myb, negatively regulates ABA-induced inhibition of seed germination by blocking the expression of the bZIP transcription factor ABI5.Crossref | GoogleScholarGoogle Scholar |

Li C, Ng C, Fan L (2015) MYB transcription factors, active players in abiotic stress signaling. Environmental and Experimental Botany 114, 80–91.
MYB transcription factors, active players in abiotic stress signaling.Crossref | GoogleScholarGoogle Scholar |

Li M, Dong X, Peng J, Xu W, Ren R, Liu J, Cao F, Liu Z (2016) De novo transcriptome sequencing and gene expression analysis reveal potential mechanisms of seed abortion in dove tree (Davidia involucrata Baill.). BMC Plant Biology 16, 82
De novo transcriptome sequencing and gene expression analysis reveal potential mechanisms of seed abortion in dove tree (Davidia involucrata Baill.).Crossref | GoogleScholarGoogle Scholar | 27068221PubMed |

Long Z, Gichira A, Chen J, Wang Q, Liao K (2016) Development of EST-SSR markers in the relict tree Davidia involucrata (Davidiaceae) using transcriptome sequencing. Genetics and Molecular Research 15,
Development of EST-SSR markers in the relict tree Davidia involucrata (Davidiaceae) using transcriptome sequencing.Crossref | GoogleScholarGoogle Scholar | 27813565PubMed |

Machado A, Wu Y, Yang Y, Llewellyn D, Dennis E (2009) The MYB transcription factor GhMYB25 regulates early fibre and trichome development. The Plant Journal 59, 52–62.
The MYB transcription factor GhMYB25 regulates early fibre and trichome development.Crossref | GoogleScholarGoogle Scholar | 19309462PubMed |

Magome H, Yamaguchi S, Hanada A, Kamiya Y, Oda K (2004) Dwarf and delayed-flowering 1, a novel Arabidopsis mutant deficient in gibberellin biosynthesis because of overexpression of a putative AP2 transcription factor. The Plant Journal 37, 720–729.
Dwarf and delayed-flowering 1, a novel Arabidopsis mutant deficient in gibberellin biosynthesis because of overexpression of a putative AP2 transcription factor.Crossref | GoogleScholarGoogle Scholar | 14871311PubMed |

Manchester SR (2002) Leaves and fruits of Davidia (Cornales) from the Paleocene of North America. Systematic Botany 27, 368–382.
Leaves and fruits of Davidia (Cornales) from the Paleocene of North America.Crossref | GoogleScholarGoogle Scholar |

Murashige T, Skoog F (1962) A revised medium for rapid growth and bio assays with tobacco tissue cultures. Physiologia Plantarum 15, 473–497.
A revised medium for rapid growth and bio assays with tobacco tissue cultures.Crossref | GoogleScholarGoogle Scholar |

Nesi N, Jond C, Debeaujon I, Caboche M, Lepiniec L (2001) The Arabidopsis TT2 gene encodes an R2R3 MYB domain protein that acts as a key determinant for proanthocyanidin accumulation in developing seed. The Plant Cell 13, 2099–2114.
The Arabidopsis TT2 gene encodes an R2R3 MYB domain protein that acts as a key determinant for proanthocyanidin accumulation in developing seed.Crossref | GoogleScholarGoogle Scholar | 11549766PubMed |

Newman L, Perazza D, Juda L, Campbell M (2003) Involvement of the R2R3–MYB, AtMYB61, in the ectopic lignification and dark-photomorphogenic components of the det3 mutant phenotype. The Plant Journal 37, 239–250.
Involvement of the R2R3–MYB, AtMYB61, in the ectopic lignification and dark-photomorphogenic components of the det3 mutant phenotype.Crossref | GoogleScholarGoogle Scholar |

Nguyen X, Hoang M, Kim H, Lee K, Liu X, Kim S, Bahk S, Park H, Chung W (2012) Phosphorylation of the transcriptional regulator MYB44 by mitogen activated protein kinase regulates Arabidopsis seed germination. Biochemical and Biophysical Research Communications 423, 703–708.
Phosphorylation of the transcriptional regulator MYB44 by mitogen activated protein kinase regulates Arabidopsis seed germination.Crossref | GoogleScholarGoogle Scholar | 22704933PubMed |

Niu W, Zhang T, Deng D, Zhuang W (2013) A review on reproductive technology and growing of Davidia involucrata Baill. Plant Physiology Communications 49, 50–54.
A review on reproductive technology and growing of Davidia involucrata Baill.Crossref | GoogleScholarGoogle Scholar |

Qi T, Huang H, Song S, Xie D (2015) Regulation of jasmonate-mediated stamen development and seed production by a bHLH–MYB complex in Arabidopsis. The Plant Cell 27, 1620–1633.
Regulation of jasmonate-mediated stamen development and seed production by a bHLH–MYB complex in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 26002869PubMed |

Ren R, Huang F, Gao R, Dong X, Peng J, Cao F, Li M (2019) Selection and validation of suitable reference genes for RT-qPCR analysis in dove tree (Davidia involucrata Baill.) Trees 33, 837–849.
Selection and validation of suitable reference genes for RT-qPCR analysis in dove tree (Davidia involucrata Baill.)Crossref | GoogleScholarGoogle Scholar |

Reyes J, Chua N (2007) ABA induction of miR159 controls transcript levels of two MYB factors during Arabidopsis seed germination. The Plant Journal 49, 592–606.
ABA induction of miR159 controls transcript levels of two MYB factors during Arabidopsis seed germination.Crossref | GoogleScholarGoogle Scholar | 17217461PubMed |

Ruan Y, Patrick J, Bouzayen M, Osorio S, Fernie A (2012) Molecular regulation of seed and fruit set. Trends in Plant Science 17, 656–665.
Molecular regulation of seed and fruit set.Crossref | GoogleScholarGoogle Scholar | 22776090PubMed |

Shan H, Chen S, Jiang J, Chen F, Chen Y, Gu C, Li P, Song A, Zhu X, Gao H (2012) Heterologous expression of the chrysanthemum R2R3–MYB transcription factor CmMYB2 enhances drought and salinity tolerance, increases hypersensitivity to ABA and delays flowering in Arabidopsis thaliana. Molecular Biotechnology 51, 160–173.
Heterologous expression of the chrysanthemum R2R3–MYB transcription factor CmMYB2 enhances drought and salinity tolerance, increases hypersensitivity to ABA and delays flowering in Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar | 21901277PubMed |

Song S, Qi T, Huang H, Ren Q, Wu D, Chang C, Peng W, Liu Y, Peng J, Xie D (2011) The jasmonate-ZIM domain proteins interact with the R2R3–MYB transcription factors MYB21 and MYB24 to affect jasmonate-regulated stamen development in Arabidopsis. The Plant Cell 23, 1000–1013.
The jasmonate-ZIM domain proteins interact with the R2R3–MYB transcription factors MYB21 and MYB24 to affect jasmonate-regulated stamen development in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 21447791PubMed |

Takos A, Jaffé F, Jacob S, Bogs J, Robinson S, Walker A (2006) Light-induced expression of a MYB gene regulates anthocyanin biosynthesis in red apples. Plant Physiology 142, 1216–1232.
Light-induced expression of a MYB gene regulates anthocyanin biosynthesis in red apples.Crossref | GoogleScholarGoogle Scholar | 17012405PubMed |

Thompson M, Ramsay R (1995) MYB: an old oncoprotein with new roles. BioEssays 17, 341–350.
MYB: an old oncoprotein with new roles.Crossref | GoogleScholarGoogle Scholar | 7741726PubMed |

Xu W, Dubos C, Lepiniec L (2015) Transcriptional control of flavonoid biosynthesis by MYB–bHLH–WDR complexes. Trends in Plant Science 20, 176–185.
Transcriptional control of flavonoid biosynthesis by MYB–bHLH–WDR complexes.Crossref | GoogleScholarGoogle Scholar | 25577424PubMed |

Yang H, Xue Q, Zhang Z, Du J, Yu D, Huang F (2018) GmMYB181, a soybean R2R3–MYB protein, increases branch number in transgenic Arabidopsis. Frontiers in Plant Science 9, 1027
GmMYB181, a soybean R2R3–MYB protein, increases branch number in transgenic Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 30065741PubMed |

Yu T, Lv J, Li J, Du F, Yin K (2016) The complete chloroplast genome of the dove tree Davidia involucrata (Nyssaceae), a relict species endemic to China. Conservation Genetics Resources 8, 263–266.
The complete chloroplast genome of the dove tree Davidia involucrata (Nyssaceae), a relict species endemic to China.Crossref | GoogleScholarGoogle Scholar |

Zhang J, Li J, Lian X (1994) Morphology and biological characteristics of Davidia involucrata. Journal of Beijing Forestry University 16, 33–37.

Zhang X, Henriques R, Lin S, Niu Q, Chua N (2006) Agrobacterium-mediated transformation of Arabidopsis thaliana using the floral dip method. Nature Protocols 1, 641–646.
Agrobacterium-mediated transformation of Arabidopsis thaliana using the floral dip method.Crossref | GoogleScholarGoogle Scholar | 17406292PubMed |

Zhang Y, Cao G, Qu L, Gu H (2009a) Characterization of Arabidopsis MYB transcription factor gene AtMYB17 and its possible regulation by LEAFY and AGL15. Journal of Genetics and Genomics 36, 99–107.
Characterization of Arabidopsis MYB transcription factor gene AtMYB17 and its possible regulation by LEAFY and AGL15.Crossref | GoogleScholarGoogle Scholar | 19232308PubMed |

Zhang Y, Cao G, Qu L, Gu H (2009b) Involvement of an R2R3–MYB transcription factor gene AtMYB118 in embryogenesis in Arabidopsis. Plant Cell Reports 28, 337–346.
Involvement of an R2R3–MYB transcription factor gene AtMYB118 in embryogenesis in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 19066902PubMed |

Zhang Y, Liang W, Shi J, Xu J, Zhang D (2013) MYB56 encoding a R2R3 MYB transcription factor regulates seed size in Arabidopsis thaliana. Journal of Integrative Plant Biology 55, 1166–1178.
MYB56 encoding a R2R3 MYB transcription factor regulates seed size in Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar | 23911125PubMed |

Zhang F, Wang Z, Dong W, Sun C, Wang H, Song A, He L, Fang W, Chen F, Teng N (2014) Transcriptomic and proteomic analysis reveals mechanisms of embryo abortion during chrysanthemum cross breeding. Scientific Reports 4, 6536
Transcriptomic and proteomic analysis reveals mechanisms of embryo abortion during chrysanthemum cross breeding.Crossref | GoogleScholarGoogle Scholar | 25288482PubMed |

Zhu X, Liang W, Cui X, Chen M, Yin C, Luo Z, Zhu J, Lucas W, Wang Z, Zhang D (2015) Brassinosteroids promote development of rice pollen grains and seeds by triggering expression of Carbon Starved Anther, a MYB domain protein. The Plant Journal 82, 570–581.
Brassinosteroids promote development of rice pollen grains and seeds by triggering expression of Carbon Starved Anther, a MYB domain protein.Crossref | GoogleScholarGoogle Scholar | 25754973PubMed |