Identification of a Sugarcane Bacilliform Virus Promoter That is Activated by Drought Stress in Plants

Overview

Journal Commun Biol

Specialty Biology

Date 2024 Mar 27

PMID 38532083

Authors

Sheng-Ren Sun

Xiao-Bin Wu

Jian-Sheng Chen

Mei-Ting Huang

Hua-Ying Fu

Qin-Nan Wang

Philippe Rott

San-Ji Gao

Affiliations

Soon will be listed here.

Abstract

Sugarcane (Saccharum spp.) is an important sugar and biofuel crop in the world. It is frequently subjected to drought stress, thus causing considerable economic losses. Transgenic technology is an effective breeding approach to improve sugarcane tolerance to drought using drought-inducible promoter(s) to activate drought-resistance gene(s). In this study, six different promoters were cloned from sugarcane bacilliform virus (SCBV) genotypes exhibiting high genetic diversity. In β-glucuronidase (GUS) assays, expression of one of these promoters (P) is similar to the one driven by the CaMV 35S promoter and >90% higher compared to the other cloned promoters and Ubi1. Three SCBV promoters (P, P, and P) function as drought-induced promoters in transgenic Arabidopsis plants. In Arabidopsis, GUS activity driven by promoter P is also upregulated by abscisic acid (ABA) and is 2.2-5.5-fold higher when compared to the same activity of two plant native promoters (P from sugarcane and P from Arabidopsis). Mutation analysis revealed that a putative promoter region 1 (PPR1) and two ABA response elements (ABREs) are required in promoter P to confer drought stress response and ABA induction. Yeast one-hybrid and electrophoretic mobility shift assays uncovered that transcription factors ScbZIP72 from sugarcane and AREB1 from Arabidopsis bind with two ABREs of promoter P. After ABA treatment or drought stress, the expression levels of endogenous ScbZIP72 and heterologous GUS are significantly increased in P:GUS transgenic sugarcane plants. Consequently, promoter P is a possible alternative promoter for genetic engineering of drought-resistant transgenic crops such as sugarcane.

References

Sun R, Han J, Zheng L, Qu F . The AC2 Protein of a Bipartite Geminivirus Stimulates the Transcription of the BV1 Gene through Abscisic Acid Responsive Promoter Elements. Viruses. 2020; 12(12). PMC: 7762296. DOI: 10.3390/v12121403. View

Mudge S, Osabe K, Casu R, Bonnett G, Manners J, Birch R . Efficient silencing of reporter transgenes coupled to known functional promoters in sugarcane, a highly polyploid crop species. Planta. 2008; 229(3):549-58. DOI: 10.1007/s00425-008-0852-8. View

Clough S, Bent A . Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J. 1999; 16(6):735-43. DOI: 10.1046/j.1365-313x.1998.00343.x. View

Rivero R, Mittler R, Blumwald E, Zandalinas S . Developing climate-resilient crops: improving plant tolerance to stress combination. Plant J. 2021; 109(2):373-389. DOI: 10.1111/tpj.15483. View

Brophy J . Toward synthetic plant development. Plant Physiol. 2021; 188(2):738-748. PMC: 8825267. DOI: 10.1093/plphys/kiab568. View

Budeguer F, Enrique R, Perera M, Racedo J, Castagnaro A, Noguera A . Genetic Transformation of Sugarcane, Current Status and Future Prospects. Front Plant Sci. 2021; 12:768609. PMC: 8632530. DOI: 10.3389/fpls.2021.768609. View

Shrestha A, Cudjoe D, Kamruzzaman M, Siddique S, Fiorani F, Leon J . Abscisic acid-responsive element binding transcription factors contribute to proline synthesis and stress adaptation in Arabidopsis. J Plant Physiol. 2021; 261:153414. DOI: 10.1016/j.jplph.2021.153414. View

Aono A, Pimenta R, Garcia A, Correr F, Hosaka G, Carrasco M . The Wild Sugarcane and Sorghum Kinomes: Insights Into Expansion, Diversification, and Expression Patterns. Front Plant Sci. 2021; 12:668623. PMC: 8294386. DOI: 10.3389/fpls.2021.668623. View

Todaka D, Shinozaki K, Yamaguchi-Shinozaki K . Recent advances in the dissection of drought-stress regulatory networks and strategies for development of drought-tolerant transgenic rice plants. Front Plant Sci. 2015; 6:84. PMC: 4332304. DOI: 10.3389/fpls.2015.00084. View

10.

Gao S, Damaj M, Park J, Wu X, Sun S, Chen R . A novel promoter confers gene expression preferentially in the vascular bundle and storage parenchyma of the sugarcane culm. Biotechnol Biofuels. 2017; 10:172. PMC: 5496340. DOI: 10.1186/s13068-017-0850-9. View

11.

Liu J, Shu D, Tan Z, Ma M, Guo N, Gao S . The Arabidopsis IDD14 transcription factor interacts with bZIP-type ABFs/AREBs and cooperatively regulates ABA-mediated drought tolerance. New Phytol. 2022; 236(3):929-942. DOI: 10.1111/nph.18381. View

12.

Liu W, Stewart Jr C . Plant synthetic promoters and transcription factors. Curr Opin Biotechnol. 2015; 37:36-44. DOI: 10.1016/j.copbio.2015.10.001. View

13.

Jores T, Tonnies J, Wrightsman T, Buckler E, Cuperus J, Fields S . Synthetic promoter designs enabled by a comprehensive analysis of plant core promoters. Nat Plants. 2021; 7(6):842-855. PMC: 10246763. DOI: 10.1038/s41477-021-00932-y. View

14.

Liu Y, Yang T, Lin Z, Gu B, Xing C, Zhao L . A WRKY transcription factor PbrWRKY53 from Pyrus betulaefolia is involved in drought tolerance and AsA accumulation. Plant Biotechnol J. 2019; 17(9):1770-1787. PMC: 6686137. DOI: 10.1111/pbi.13099. View

15.

Fujita Y, Fujita M, Satoh R, Maruyama K, Parvez M, Seki M . AREB1 is a transcription activator of novel ABRE-dependent ABA signaling that enhances drought stress tolerance in Arabidopsis. Plant Cell. 2005; 17(12):3470-88. PMC: 1315382. DOI: 10.1105/tpc.105.035659. View

16.

Wang Y, Hou Y, Qiu J, Wang H, Wang S, Tang L . Abscisic acid promotes jasmonic acid biosynthesis via a 'SAPK10-bZIP72-AOC' pathway to synergistically inhibit seed germination in rice (Oryza sativa). New Phytol. 2020; 228(4):1336-1353. PMC: 7689938. DOI: 10.1111/nph.16774. View

17.

Ying S, Zhang D, Fu J, Shi Y, Song Y, Wang T . Cloning and characterization of a maize bZIP transcription factor, ZmbZIP72, confers drought and salt tolerance in transgenic Arabidopsis. Planta. 2011; 235(2):253-66. DOI: 10.1007/s00425-011-1496-7. View

18.

Ghorbani Faal P, Farsi M, Seifi A, Kakhki A . Virus-induced CRISPR-Cas9 system improved resistance against tomato yellow leaf curl virus. Mol Biol Rep. 2020; 47(5):3369-3376. DOI: 10.1007/s11033-020-05409-3. View

19.

Javed T, Gao S . WRKY transcription factors in plant defense. Trends Genet. 2023; 39(10):787-801. DOI: 10.1016/j.tig.2023.07.001. View

20.

Javed T, Shabbir R, Ali A, Afzal I, Zaheer U, Gao S . Transcription Factors in Plant Stress Responses: Challenges and Potential for Sugarcane Improvement. Plants (Basel). 2020; 9(4). PMC: 7238037. DOI: 10.3390/plants9040491. View