Physiological and Transcriptome Analysis of the Effects of Exogenous Strigolactones on Drought Responses of Pepper Seedlings
Abstract
:1. Introduction
2. Materials and Methods
2.1. Plant Materials and Treatments
2.2. Measurement of Relative Water Content and Root Morphology
2.3. Scanning Electron Microscopy
2.4. Chlorophyll Content
2.5. Measurement of Antioxidant Enzyme Activity and Related Metabolites
2.6. Transcriptome Sequencing, Differential Gene Expression, and Enrichment Analysis
2.7. Gene Expression by qRT-PCR
2.8. Statistical Analysis
3. Results
3.1. SL Alleviated the Negative Effects of Drought Stress on the Morphology of Pepper
3.2. The Microscopic Structure of Leaf Tissue
3.3. Relative Water Content and Chlorophyll Content of the Leaves
3.4. Measurement of Antioxidant Enzyme Activity and Related Metabolites
3.5. Assessment of RNA-Seq Data and Differentially Expressed Gene Analysis
3.6. Enrichment Analysis of DEGs
3.7. Candidate Genes Involved in Drought and SL Treatment
3.8. qRT-PCR Validation of Gene Expression
4. Discussion
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
- Nadeem, M.; Li, J.; Yahya, M.; Sher, A.; Ma, C.; Wang, X.; Qiu, L. Research progress and perspective on drought stress in legumes: A review. Int. J. Mol. Sci. 2019, 20, 2541. [Google Scholar] [CrossRef] [PubMed]
- Giordano, D.; Provenzano, S.; Ferrandino, A.; Vitali, M.; Pagliarani, C.; Roman, F.; Cardinale, F.; Castellarin, S.D.; Schubert, A. Characterization of a multifunctional caffeoyl-CoA O-methyltransferase activated in grape berries upon drought stress. Plant Physiol. Biochem. 2016, 101, 23–32. [Google Scholar] [CrossRef]
- Qin, C.; Yu, C.; Shen, Y.; Fang, X.; Chen, L.; Min, J.; Cheng, J.; Zhao, S.; Xu, M.; Luo, Y.; et al. Whole-genome sequencing of cultivated and wild peppers provides insights into Capsicum domestication and specialization. Proc. Natl. Acad. Sci. USA 2014, 111, 5135–5140. [Google Scholar] [CrossRef] [PubMed]
- Manivannan, A.; Kim, J.H.; Yang, E.Y.; Ahn, Y.K.; Lee, E.S.; Choi, S.; Kim, D.S. Next-Generation Sequencing Approaches in Genome-Wide Discovery of Single Nucleotide Polymorphism Markers Associated with Pungency and Disease Resistance in Pepper. Biomed Res. Int. 2018, 2018, 5646213. [Google Scholar] [CrossRef]
- Gomez-Roldan, V.; Fermas, S.; Brewer, P.B.; Puech-Pagès, V.; Dun, E.A.; Pillot, J.P.; Letisse, F.; Matusova, R.; Danoun, S.; Portais, J.C.; et al. Strigolactone inhibition of shoot branching. Nature 2008, 455, 189–194. [Google Scholar] [CrossRef]
- Waters, M.T.; Gutjahr, C.; Bennett, T.; Nelson, D.C. Strigolactone Signaling and Evolution. Annu. Rev. Plant Biol. 2017, 68, 291–322. [Google Scholar] [CrossRef] [PubMed]
- Chesterfield, R.J.; Vickers, C.E.; Beveridge, C.A. Translation of strigolactones from plant hormone to agriculture: Achievements, future perspectives, and challenges. Trends. Plant. Sci. 2020, 25, 1087–1106. [Google Scholar] [CrossRef]
- Min, Z.; Li, R.; Chen, L.; Zhang, Y.; Li, Z.; Liu, M.; Ju, Y.; Fang, Y. Alleviation of drought stress in grapevine by foliar-applied strigolactones. Plant Physiol. Biochem. 2019, 135, 99–110. [Google Scholar] [CrossRef]
- Visentin, I.; Vitali, M.; Ferrero, M.; Zhang, Y.; Ruyter-Spira, C.; Novák, O.; Strnad, M.; Lovisolo, C.; Schubert, A.; Cardinale, F. Low levels of strigolactones in roots as a component of the systemic signal of drought stress in tomato. New Phytol. 2016, 212, 954–963. [Google Scholar] [CrossRef]
- Ha, C.V.; Leyva-González, M.A.; Osakabe, Y.; Tran, U.T.; Nishiyama, R.; Watanabe, Y.; Tanaka, M.; Seki, M.; Yamaguchi, S.; Dong, N.V.; et al. Positive regulatory role of strigolactone in plant responses to drought and salt stress. Proc. Natl. Acad. Sci. USA 2014, 111, 851–856. [Google Scholar] [CrossRef] [PubMed]
- Wang, Q.; Ni, J.; Shah, F.; Liu, W.; Wang, D.; Yao, Y.; Hu, H.; Huang, S.; Hou, J.; Fu, S.; et al. Overexpression of the stress-Inducible SsMAX2 promotes drought and dalt resistance via the regulation of redox homeostasis in Arabidopsis. Int. J. Mol. Sci. 2019, 20, 837. [Google Scholar] [CrossRef] [PubMed]
- Altaf, M.A.; Hao, Y.; He, C.; Mumtaz, M.A.; Shu, H.; Fu, H.; Wang, Z. Physiological and biochemical responses of Ppepper (Capsicum annuum L.) seedlings to nickel toxicity. Front. Plant Sci. 2022, 13, 950392. [Google Scholar] [CrossRef] [PubMed]
- Kim, D.; Langmead, B.; Salzberg, S.L. HISAT: A fast spliced aligner with low memory requirements. Nat. Methods 2015, 12, 357–360. [Google Scholar] [CrossRef] [PubMed]
- Love, M.I.; Huber, W.; Anders, S. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol. 2014, 15, 550. [Google Scholar] [CrossRef]
- Young, M.D.; Wakefield, M.J.; Smyth, G.K.; Oshlack, A. Gene ontology analysis for RNA-seq: Accounting for selection bias. Genome Biol. 2010, 11, R14. [Google Scholar] [CrossRef]
- Kanehisa, M.; Goto, S. KEGG: Kyoto encyclopedia of genes and genomes. Nucleic Acids Res. 2000, 28, 27–30. [Google Scholar] [CrossRef]
- Shu, H.; Zhang, Y.; He, C.; Altaf, M.A.; Hao, Y.; Liao, D.; Li, L.; Li, C.; Fu, H.; Cheng, S.; et al. Establishment of in vitro regeneration system and molecular analysis of early development of somatic callus in Capsicum chinense and Capsicum baccatum. Front. Plant Sci. 2022, 13, 1025497. [Google Scholar] [CrossRef]
- Kaya, C.; Ashraf, M.; Wijaya, L.; Ahmad, P. The putative role of endogenous nitric oxide in brassinosteroid-induced antioxidant defence system in pepper (Capsicum annuum L.) plants under water stress. Plant Physiol. Biochem. 2019, 143, 119–128. [Google Scholar] [CrossRef]
- Salvi, P.; Manna, M.; Kaur, H.; Thakur, T.; Gandass, N.; Bhatt, D.; Muthamilarasan, M. Phytohormone signaling and crosstalk in regulating drought stress response in plants. Plant Cell Rep. 2021, 40, 1305–1329. [Google Scholar] [CrossRef]
- Saeed, W.; Naseem, S.; Ali, Z. Strigolactones biosynthesis and their role in abiotic stress resilience in plants: A critical review. Front. Plant Sci. 2017, 8, 1487. [Google Scholar] [CrossRef] [PubMed]
- Liu, B.; Zhang, Y.; Wang, S.; Wang, W.; Xu, X.; Wu, J.; Fang, Y.; Ju, Y. Effects of strigolactone and abscisic acid on the quality and antioxidant activity of grapes (Vitis vinifera L.) and wines. Food Chem. X 2022, 16, 100496. [Google Scholar] [CrossRef] [PubMed]
- Mahmood, T.; Khalid, S.; Abdullah, M.; Ahmed, Z.; Shah, M.K.N.; Ghafoor, A.; Du, X. Insights into drought Stress dignaling in plants and the molecular genetic Basis of cotton drought tolerance. Cells 2019, 9, 105. [Google Scholar] [CrossRef] [PubMed]
- Kalaji, H.M.; Jajoo, A.; Oukarroum, A.; Brestic, M.; Zivcak, M.; Samborska, I.A.; Cetner, M.D.; Łukasik, I.; Goltsev, V.; Ladle, R.J. Chlorophyll a fluorescence as a tool to monitor physiological status of plants under abiotic stress conditions. Acta Physiol. Plant. 2016, 38, 1–11. [Google Scholar] [CrossRef]
- Ozturk, M.; Turkyilmaz Unal, B.; García-Caparrós, P.; Khursheed, A.; Gul, A.; Hasanuzzaman, M. Osmoregulation and its actions during the drought stress in plants. Physiol. Plant 2021, 172, 1321–1335. [Google Scholar] [CrossRef]
- Müller, M.; Munné-Bosch, S. Hormonal impact on photosynthesis and photoprotection in plants. Plant Physiol. 2021, 185, 1500–1522. [Google Scholar] [CrossRef] [PubMed]
- Wang, W.N.; Min, Z.; Wu, J.R.; Liu, B.C.; Xu, X.L.; Fang, Y.L.; Ju, Y.L. Physiological and transcriptomic analysis of Cabernet Sauvginon (Vitis vinifera L.) reveals the alleviating effect of exogenous strigolactones on the response of grapevine to drought stress. Plant Physiol. Biochem. 2021, 167, 400–409. [Google Scholar] [CrossRef]
- Szabados, L.; Savouré, A. Proline: A multifunctional amino acid. Trends. Plant Sci. 2010, 15, 89–97. [Google Scholar] [CrossRef]
- Bandurska, H.; Niedziela, J.; Pietrowska-Borek, M.; Nuc, K.; Chadzinikolau, T.; Radzikowska, D. Regulation of proline biosynthesis and resistance to drought stress in two barley (Hordeum vulgare L.) genotypes of different origin. Plant Physiol. Biochem. 2017, 118, 427–437. [Google Scholar] [CrossRef] [PubMed]
- Fichman, Y.; Gerdes, S.Y.; Kovács, H.; Szabados, L.; Zilberstein, A.; Csonka, L.N. Evolution of proline biosynthesis: Enzymology, bioinformatics, genetics, and transcriptional regulation. Biol. Rev. Camb. Philos. Soc. 2015, 90, 1065–1099. [Google Scholar] [CrossRef]
- Sharma, A.; Zheng, B. Melatonin mediated regulation of drought stress: Physiological and molecular aspects. Plants 2019, 8, 190. [Google Scholar] [CrossRef]
- Yao, Y.; Liu, X.; Li, Z.; Ma, X.; Rennenberg, H.; Wang, X.; Li, H. Drought-induced H2O2 accumulation in subsidiary cells is involved in regulatory signaling of stomatal closure in maize leaves. Planta 2013, 238, 217–227. [Google Scholar] [CrossRef]
- Ding, Z.J.; Yan, J.Y.; Xu, X.Y.; Yu, D.Q.; Li, G.X.; Zhang, S.Q.; Zheng, S.J. Transcription factor WRKY46 regulates osmotic stress responses and stomatal movement independently in Arabidopsis. Plant J. 2014, 79, 13–27. [Google Scholar] [CrossRef]
- Ahmad, S.; Kamran, M.; Ding, R.; Meng, X.; Wang, H.; Ahmad, I.; Fahad, S.; Han, Q. Exogenous melatonin confers drought stress by promoting plant growth, photosynthetic capacity and antioxidant defense system of maize seedlings. PeerJ 2019, 7, e7793. [Google Scholar] [CrossRef]
- Qiu, C.W.; Zhang, C.; Wang, N.H.; Mao, W.; Wu, F. Strigolactone GR24 improves cadmium tolerance by regulating cadmium uptake, nitric oxide signaling and antioxidant metabolism in barley (Hordeum vulgare L.). Environ. Pollut. 2021, 273, 116486. [Google Scholar] [CrossRef]
- Gururani, M.A.; Mohanta, T.K.; Bae, H. Current understanding of the interplay between phytohormones and photosynthesis under environmental stress. Int. J. Mol. Sci. 2015, 16, 19055–19085. [Google Scholar] [CrossRef] [PubMed]
- Gupta, A.; Rico-Medina, A.; Caño-Delgado, A.I. The physiology of plant responses to drought. Science 2020, 368, 266–269. [Google Scholar] [CrossRef]
- Nam, M.H.; Huh, S.M.; Kim, K.M.; Park, W.J.; Seo, J.B.; Cho, K.; Kim, D.Y.; Kim, B.G.; Yoon, I.S. Comparative proteomic analysis of early salt stress-responsive proteins in roots of SnRK2 transgenic rice. Proteome Sci. 2012, 10, 25. [Google Scholar] [CrossRef] [PubMed]
- Luo, J.; Zhou, J.J.; Zhang, J.Z. Aux/IAA gene family in plants: Molecular structure, regulation, and function. Int. J. Mol. Sci. 2018, 19, 259. [Google Scholar] [CrossRef]
- Nguyen, H.T.; Umemura, K.; Kawano, T. Indole-3-acetic acid-induced oxidative burst and an increase in cytosolic calcium ion concentration in rice suspension culture. Biosci. Biotechnol. Biochem. 2016, 80, 1546–1554. [Google Scholar] [CrossRef] [PubMed]
- Kretzschmar, T.; Burla, B.; Lee, Y.; Martinoia, E.; Nagy, R. Functions of ABC transporters in plants. Essays Biochem. 2011, 50, 145–160. [Google Scholar] [CrossRef]
- Kim, D.Y.; Jin, J.Y.; Alejandro, S.; Martinoia, E.; Lee, Y. Overexpression of AtABCG36 improves drought and salt stress resistance in Arabidopsis. Physiol. Plant 2010, 139, 170–180. [Google Scholar] [CrossRef] [PubMed]
- Wang, L.; Wang, B.; Jiang, L.; Liu, X.; Li, X.; Lu, Z.; Meng, X.; Wang, Y.; Smith, S.M.; Li, J. Strigolactone signaling in Arabidopsis regulates shoot development by targeting D53-Like SMXL repressor proteins for ubiquitination and degradation. Plant Cell 2015, 27, 3128–3142. [Google Scholar] [CrossRef]
- Yao, R.; Ming, Z.; Yan, L.; Li, S.; Wang, F.; Ma, S.; Yu, C.; Yang, M.; Chen, L.; Chen, L.; et al. DWARF14 is a non-canonical hormone receptor for strigolactone. Nature 2016, 536, 469–473. [Google Scholar] [CrossRef] [PubMed]
- Bu, Q.; Lv, T.; Shen, H.; Luong, P.; Wang, J.; Wang, Z.; Huang, Z.; Xiao, L.; Engineer, C.; Kim, T.H.; et al. Regulation of drought tolerance by the F-box protein MAX2 in Arabidopsis. Plant Physiol. 2014, 164, 424–439. [Google Scholar] [CrossRef] [PubMed]
- Yang, T.; Lian, Y.; Kang, J.; Bian, Z.; Xuan, L.; Gao, Z.; Wang, X.; Deng, J.; Wang, C. The SUPPRESSOR of MAX2 1 (SMAX1)-Like SMXL6, SMXL7 and SMXL8 act as negative regulators in response to drought stress in Arabidopsis. Plant Cell Physiol. 2020, 61, 1477–1492. [Google Scholar] [CrossRef]
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Shu, H.; Altaf, M.A.; Mushtaq, N.; Fu, H.; Lu, X.; Zhu, G.; Cheng, S.; Wang, Z. Physiological and Transcriptome Analysis of the Effects of Exogenous Strigolactones on Drought Responses of Pepper Seedlings. Antioxidants 2023, 12, 2019. https://doi.org/10.3390/antiox12122019
Shu H, Altaf MA, Mushtaq N, Fu H, Lu X, Zhu G, Cheng S, Wang Z. Physiological and Transcriptome Analysis of the Effects of Exogenous Strigolactones on Drought Responses of Pepper Seedlings. Antioxidants. 2023; 12(12):2019. https://doi.org/10.3390/antiox12122019
Chicago/Turabian StyleShu, Huangying, Muhammad Ahsan Altaf, Naveed Mushtaq, Huizhen Fu, Xu Lu, Guopeng Zhu, Shanhan Cheng, and Zhiwei Wang. 2023. "Physiological and Transcriptome Analysis of the Effects of Exogenous Strigolactones on Drought Responses of Pepper Seedlings" Antioxidants 12, no. 12: 2019. https://doi.org/10.3390/antiox12122019