Strigolactones Might Regulate Ovule Development after Fertilization in Xanthoceras sorbifolium
Abstract
:1. Introduction
2. Results
2.1. The Presence of Strigolactones in Ovules after Fertilization and the Effect of Exogenous Pi Application on Their Content
2.2. Effect of Exogenous Application of GR24 and TIS108 on Fruit Set and Early Seed Development
2.3. Genome-Wide Identification of SL Biosynthesis Genes and Their Expression in Normally and Abnormally Developing Ovules after Fertilization
2.4. Genome-Wide Identification of Genes Related to SL Perception and Signaling and Their Expression in Fertilized Ovules
2.5. Genome-Wide Identification of Xanthoceras Invertase Genes and Crosstalk between Sugar and Strigolactone in the Development of Fertilized Ovules
2.6. Silencing of the XsD14 Gene Promoted Early Seed Development
3. Discussion
4. Materials and Methods
4.1. Plant Materials
4.2. Histological Analysis
4.3. Strigolactone Analysis
4.4. Soluble Sugar Analysis
4.5. Invertase Enzyme Assay
4.6. Assays of GR24 and TIS108 Treatment
4.7. Assays of Sucrose Treatment
4.8. Phosphorus (P) Applications
4.9. RNA Extraction, Library Construction, and Illumina Sequencing
4.10. RNA-Seq Data Analysis
4.11. Real-Time qRT-PCR Analysis
4.12. Virus-Induced Gene Silence (VIGS) Assays
4.13. Statistical Analysis
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
- Brewer, P.B.; Koltai, H.; Beveridge, C.A. Diverse roles of strigolactones in plant development. Mol. Plant 2013, 6, 18–28. [Google Scholar] [CrossRef] [PubMed]
- 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]
- Marzec, M.; Melzer, M. Regulation of root development and architecture by strigolactones under optimal and nutrient deficiency conditions. Int. J. Mol. Sci. 2018, 19, 1887. [Google Scholar] [CrossRef]
- Elhiti, M.; Mira, M.M.; So, K.K.Y.; Stasolla, C.; Hebelstrup, K.H. Synthetic strigolactone GR24 improves Arabidopsis somatic embryogenesis through changes in auxin responses. Plants 2021, 10, 2720. [Google Scholar] [CrossRef] [PubMed]
- Yamada, Y.; Furusawa, S.; Nagasaka, S.; Shimomura, K.; Yamaguchi, S.; Umehara, M. Strigolactone signaling regulates rice leaf senescence in response to a phosphate deficiency. Planta 2014, 240, 399–408. [Google Scholar] [CrossRef]
- Xu, X.; Jibran, R.; Wang, Y.T.; Dong, L.M.; Flokova, K.; Esfandiari, A.; McLachlan, A.R.G.; Heiser, A.; Sutherland-Smith, A.J.; Brummell, D.A.; et al. Strigolactones regulate sepal senescence in Arabidopsis. J. Exp. Bot. 2021, 72, 5462–5477. [Google Scholar] [CrossRef]
- Yoneyama, K.; Xie, X.N.; Kim, H.I.; Kisugi, T.; Nomura, T.; Sekimoto, H.; Yokota, T.; Yoneyama, K. How do nitrogen and phosphorus deficiencies affect strigolactone production and exudation? Planta 2012, 235, 1197–1207. [Google Scholar] [CrossRef] [PubMed]
- Van Ha, C.; Leyva-González, M.A.; Osakabe, Y.; Tran, U.T.; Nishiyama, R.; Watanabe, Y.; Tanaka, M.; Seki, M.; Yamaguchi, S.; Van Dong, N.; 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]
- Cook, C.E.; Whichard, L.P.; Turner, B.; Wall, M.E.; Egley, G.H. Germination of witchweed (Striga lutea Lour.): Isolation and properties of a potent stimulant. Science 1966, 154, 1189–1190. [Google Scholar] [CrossRef]
- Wakabayashi, T.; Ishiwa, S.; Shida, K.; Motonami, N.; Suzuki, H.; Takikawa, H.; Mizutani, M.; Sugimoto, Y. Identification and characterization of sorgomol synthase in sorghum strigolactone biosynthesis. Plant Physiol. 2021, 185, 902–913. [Google Scholar] [CrossRef]
- Czarnecki, O.; Yang, J.; Weston, D.J.; Tuskan, G.A.; Chen, J.G. A dual role of strigolactones in phosphate acquisition and utilization in plants. Int. J. Mol. Sci. 2013, 14, 7681–7701. [Google Scholar] [CrossRef]
- Gamir, J.; Torres-Vera, R.; Rial, C.; Berrio, E.; de Souza Campos, P.M.; Varela, R.M.; Macías, F.A.; Pozo, M.J.; Flors, V.; López-Ráez, J.A. Exogenous strigolactones impact metabolic profiles and phosphate starvation signalling in roots. Plant Cell Environ. 2020, 43, 1655–1668. [Google Scholar] [CrossRef]
- Woo, H.R.; Chung, K.M.; Park, J.H.; Oh, S.A.; Ahn, T.; Hong, S.H.; Jang, S.K.; Nam, H.G. ORE9, an F-box protein that regulates leaf senescence in Arabidopsis. Plant Cell 2001, 13, 1779–1790. [Google Scholar] [CrossRef]
- Stirnberg, P.; van De Sande, K.; Leyser, H.M. MAX1 and MAX2 control shoot lateral branching in Arabidopsis. Development 2002, 129, 1131–1141. [Google Scholar] [CrossRef]
- Booker, J.; Auldridge, M.; Wills, S.; McCarty, D.; Klee, H.; Leyser, O. MAX3/CCD7 is a carotenoid cleavage dioxygenase required for the synthesis of a novel plant signaling molecule. Curr. Biol. 2004, 14, 1232–1238. [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]
- Brewer, P.B.; Yoneyama, K.; Filardo, F.; Meyers, E.; Scaffidi, A.; Frickey, T.; Akiyama, K.; Seto, Y.; Dun, E.A.; Cremer, J.E.; et al. LATERAL BRANCHING OXIDOREDUCTASE acts in the final stages of strigolactone biosynthesis in Arabidopsis. Proc. Natl. Acad. Sci. USA 2016, 113, 6301–6306. [Google Scholar] [CrossRef]
- Beveridge, C.A.; Ross, J.J.; Murfet, I.C. Branching mutant rms-2 in Pisum sativun. Plant Physiol. 1994, 104, 953–959. [Google Scholar] [CrossRef]
- Beveridge, C.A.; Symons, G.M.; Murfet, I.C.; Ross, J.J.; Rameau, C. The rms1 mutant of pea has elevated indole-3-acetic acid levels and reduced root-sap zeatin riboside content but increased branching controlled by graft-transmissible signal(s). Plant Physiol. 1997, 115, 1251–1258. [Google Scholar] [CrossRef]
- Morris, S.E.; Turnbull, C.G.; Murfet, I.C.; Beveridge, C.A. Mutational analysis of branching in pea. Evidence that Rms1 and Rms5 regulate the same novel signal. Plant Physiol. 2001, 126, 1205–1213. [Google Scholar] [CrossRef]
- Napoli, C. Highly branched phenotype of the petunia dad1-1 mutant is reversed by grafting. Plant Physiol. 1996, 111, 27–37. [Google Scholar] [CrossRef]
- Snowden, K.C.; Simkin, A.J.; Janssen, B.J.; Templeton, K.R.; Loucas, H.M.; Simons, J.L.; Karunairetnam, S.; Gleave, A.P.; Clark, D.G.; Klee, H.J. The decreased apical dominance1/Petunia hybrida carotenoid cleavage dioxygenase8 gene affects branch production and plays a role in leaf senescence, root growth, and flower development. Plant Cell 2005, 17, 746–759. [Google Scholar] [CrossRef] [PubMed]
- Zhou, F.; Lin, Q.B.; Zhu, L.H.; Ren, Y.L.; Zhou, K.N.; Shabek, N.; Wu, F.; Mao, H.; Dong, W.; Gan, L.; et al. D14-SCFD3-dependent degradation of D53 regulates strigolactone signalling. Nature 2013, 504, 406–410. [Google Scholar] [CrossRef]
- Haider, I.; Andreo-Jimenez, B.; Bruno, M.; Bimbo, A.; Floková, K.; Abuauf, H.; Ntui, V.O.; Guo, X.; Charnikhova, T.; Al-Babili, S.; et al. The interaction of strigolactones with abscisic acid during the drought response in rice. J. Exp. Bot. 2018, 69, 2403–2414. [Google Scholar] [CrossRef]
- Flematti, G.R.; Scaffidi, A.; Waters, M.T.; Smith, S.M. Stereospecificity in strigolactone biosynthesis and perception. Planta 2016, 243, 1361–1373. [Google Scholar] [CrossRef]
- Arite, T.; Umehara, M.; Ishikawa, S.; Hanada, A.; Maekawa, M.; Yamaguchi, S.; Kyozuka, J. d14, a strigolactone-insensitive mutant of rice, shows an accelerated outgrowth of tillers. Plant Cell Physiol. 2009, 50, 1416–1424. [Google Scholar] [CrossRef]
- Waters, M.T.; Nelson, D.C.; Scaffidi, A.; Flematti, G.R.; Sun, Y.K.; Dixon, K.W.; Smith, S.M. Specialisation within the DWARF14 protein family confers distinct responses to karrikins and strigolactones in Arabidopsis. Development 2012, 139, 1285–1295. [Google Scholar] [CrossRef]
- de Saint Germain, A.; Clavé, G.; Badet-Denisot, M.-A.; Pillot, J.-P.; Cornu, D.; Le Caer, J.-P.; Burger, M.; Pelissier, F.; Retailleau, P.; Turnbull, C.; et al. An histidine covalent receptor and butenolide complex mediates strigolactone perception. Nature Chem. Biol. 2016, 12, 787–794. [Google Scholar] [CrossRef] [PubMed]
- Hamiaux, C.; Drummond, R.S.; Janssen, B.J.; Ledger, S.E.; Cooney, J.M.; Newcomb, R.D.; Snowden, K.C. DAD2 is an alpha/beta hydrolase likely to be involved in the perception of the plant branching hormone, strigolactone. Curr. Biol. 2012, 22, 2032–2036. [Google Scholar] [CrossRef]
- Yao, R.; Wang, L.; Li, Y.; Chen, L.; Li, S.; Du, X.; Wang, B.; Yan, J.; Li, J.; Xie, D. Rice DWARF14 acts as an unconventional hormone receptor for strigolactone. J. Exp. Bot. 2018, 69, 2355–2365. [Google Scholar] [CrossRef] [PubMed]
- Shabek, N.; Ticchiarelli, F.; Mao, H.B.; Hinds, T.R.; Leyser, O.; Zheng, N. Structural plasticity of D3-D14 ubiquitin ligase in strigolactone signalling. Nature 2018, 563, 652–656. [Google Scholar] [CrossRef]
- Jeandet, P.; Formela-Luboińska, M.; Labudda, M.; Morkunas, I. The role of sugars in plant responses to stress and their regulatory function during development. Int. J. Mol. Sci. 2022, 23, 5161. [Google Scholar] [CrossRef]
- Fichtner, F.; Barbier, F.F.; Annunziata, M.G.; Feil, R.; Olas, J.J.; Mueller-Roeber, B.; Stitt, M.; Beveridge, C.A.; Lunn, J.E. Regulation of shoot branching in arabidopsis by trehalose 6-phosphate. New Phytol. 2021, 229, 2135–2151. [Google Scholar] [CrossRef] [PubMed]
- Mishra, B.S.; Singh, M.; Aggrawal, P.; Laxmi, A. Glucose and auxin signaling interaction in controlling Arabidopsis thaliana seedlings root growth and development. PLoS ONE 2009, 4, e4502. [Google Scholar] [CrossRef] [PubMed]
- Barbier, F.F.; Cao, D.; Fichtner, F.; Weiste, C.; Perez-Garcia, M.D.; Caradeuc, M.; Le Gourrierec, J.; Sakr, S.; Beveridge, C.A. HEXOKINASE1 signalling promotes shoot branching and interacts with cytokinin and strigolactone pathways. New Phytol. 2021, 231, 1088–1104. [Google Scholar] [CrossRef] [PubMed]
- Dierck, R.; Dhooghe, E.; Van Huylenbroeck, J.; De Riek, J.; De Keyser, E.; Van Der Straeten, D. Response to strigolactone treatment in chrysanthemum axillary buds is influenced by auxin transport inhibition and sucrose availability. Acta Physiol. Plant 2016, 38, 271. [Google Scholar] [CrossRef]
- Bertheloot, J.; Barbier, F.; Boudon, F.; Perez-Garcia, M.D.; Thomas, P.; Citerne, S.; Dun, E.; Beveridge, C.; Godin, C.; Sakr, S. Sugar availability suppresses the auxin-induced strigolactone pathway to promote bud outgrowth. New Phytol. 2020, 225, 866–879. [Google Scholar] [CrossRef] [PubMed]
- Patil, S.B.; Barbier, F.F.; Zhao, J.; Zafar, S.A.; Uzair, M.; Sun, Y.L.; Fang, J.; Perez-Garcia, M.; Bertheloot, J.; Sakr, S.; et al. Sucrose promotes D53 accumulation and tillering in rice. New Phytol. 2022, 234, 122–136. [Google Scholar] [CrossRef]
- Soltani, A.; Weraduwage, S.M.; Sharkey, T.S.; Lowry, D.B. Elevated temperatures cause loss of seed set in common bean (Phaseolus vulgaris L.) potentially through the disruption of source-sink relationships. BMC Genom. 2019, 20, 312. [Google Scholar] [CrossRef]
- Trouverie, J.; Chateau-Joubert, S.; Thévenot, C.; Jacquemot, M.P.; Prioul, J.L. Regulation of vacuolar invertase by abscisic acid or glucose in leaves and roots from maize plantlets. Planta 2004, 219, 894–905. [Google Scholar] [CrossRef]
- Zhou, Q.Y.; Liu, G.S. The embryology of Xanthoceras and its phylogenetic implications. Plant Syst. Evol. 2012, 298, 457–468. [Google Scholar] [CrossRef]
- Gu, L.B.; Zhang, G.J.; Du, L.; Du, J.; Qi, K.; Zhu, X.L.; Zhang, X.Y.; Jiang, Z.H. Comparative study on the extraction of Xanthoceras sorbifolia Bunge (yellow horn) seed oil using subcritical n-butane, supercritical CO2, and the Soxhlet method. LWT-Food Sci. Technol. 2019, 111, 548–554. [Google Scholar] [CrossRef]
- Zhou, Q.Y.; Cai, Q. Role of ethylene in the regulatory mechanism underlying the abortion of ovules after fertilization in Xanthoceras sorbifolium. Plant Mol. Biol. 2021, 106, 67. [Google Scholar] [CrossRef]
- Linkies, A.; Müller, K.; Morris, K.; Turečková, V.; Wenk, M.; Cadman, C.S.; Corbineau, F.; Strnad, M.; Lynn, J.R.; Finch-Savage, W.E.; et al. Ethylene interacts with abscisic acid to regulate endosperm rupture during germination: A comparative approach using Lepidium sativum and Arabidopsis thaliana. Plant Cell 2009, 21, 3803–3822. [Google Scholar] [CrossRef] [PubMed]
- Radchuk, V.; Weier, D.; Radchuk, R.; Weschke, W.; Weber, H. Development of maternal seed tissue in barley is mediated by regulated cell expansion and cell disintegration and coordinated with endosperm growth. J. Exp. Bot. 2011, 62, 1217–1227. [Google Scholar] [CrossRef]
- Zhao, X.L.; Yang, Y.L.; Xia, H.X.; Li, Y. Genome-wide analysis of the carotenoid cleavage dioxygenases gene family in Forsythia suspensa: Expression profile and cold and drought stress responses. Front. Plant Sci. 2022, 13, 998911. [Google Scholar] [CrossRef] [PubMed]
- Mashiguchi, K.; Seto, Y.; Yamaguchi, S. Strigolactone biosynthesis, transport and perception. Plant J. 2021, 105, 335–350. [Google Scholar] [CrossRef] [PubMed]
- Kerr, S.C.; Patil, S.B.; de Saint Germain, A.; Pillot, J.P.; Saffar, J.; Ligerot, Y.; Aubert, G.; Citerne, S.; Bellec, Y.; Dun, E.A.; et al. Integration of the SMXL/D53 strigolactone signalling repressors in the model of shoot branching regulation in Pisum sativum. Plant J. 2021, 107, 1756–1770. [Google Scholar] [CrossRef]
- Ji, X.; Van den Ende, W.; Van Laere, A.; Cheng, S.; Bennett, J. Structure, evolution, and expression of the two invertase gene families of rice. J. Mol. Evol. 2005, 60, 615–634. [Google Scholar] [CrossRef]
- Zhou, Q.Y.; Zheng, Y.R.; Lai, L.M.; Du, H. Observations on sexual reproduction in Xanthoceras sorbifolium (Sapindaceae). Acta Bot. Boreal-Occident Sin. 2017, 37, 14–22. [Google Scholar]
- López-Ráez, J.A.; Bouwmeester, H. Fine-tuning regulation of strigolactone biosynthesis under phosphate starvation. Plant Signal Behav. 2008, 3, 963–965. [Google Scholar] [CrossRef]
- Aquino, B.; Bradley, J.M.; Lumba, S. On the outside looking in: Roles of endogenous and exogenous strigolactones. Plant J. 2021, 105, 322–334. [Google Scholar] [CrossRef]
- Lee, H.Y.; Yoon, G.M. Strigolactone elevates ethylene biosynthesis in etiolated Arabidopsis seedlings. Plant Signal Behav. 2020, 15, e1805232. [Google Scholar] [CrossRef]
- Matusova, R.; Rani, K.; Verstappen, F.W.A.; Franssen, M.C.R.; Beale, M.H.; Bouwmeester, H.J. The strigolactone germination stimulants of the plant-parasitic Striga and Orobanche spp. are derived from the carotenoid pathway. Plant Physiol. 2005, 139, 920–934. [Google Scholar] [CrossRef]
- Alder, A.; Jamil, M.; Marzorati, M.; Bruno, M.; Vermathen, M.; Bigler, P.; Ghisla, S.; Bouwmeester, H.; Beyer, P.; Al-Babili, S. The path from beta-carotene to carlactone, a strigolactone-like plant hormone. Science 2012, 335, 1348–1351. [Google Scholar] [CrossRef] [PubMed]
- Chevalier, F.; Nieminen, K.; Sánchez-Ferrero, J.C.; Rodríguez, M.L.; Chagoyen, M.; Hardtke, C.S.; Cubas, P. Strigolactone promotes degradation of DWARF14, an α/β hydrolase essential for strigolactone signaling in Arabidopsis. Plant Cell 2014, 26, 1134–1150. [Google Scholar] [CrossRef]
- Stanic, M.; Hickerson, N.M.N.; Arunraj, R.; Samuel, M.A. Gene-editing of the strigolactone receptor BnD14 confers promising shoot architectural changes in Brassica napus (canola). Plant Biotechnol. J. 2021, 19, 639–641. [Google Scholar] [CrossRef] [PubMed]
- Zhou, Q.Y.; Cai, Q. The superoxide dismutase genes might be required for appropriate development of the ovule after fertilization in Xanthoceras sorbifolium. Plant Cell Rep. 2018, 37, 727–739. [Google Scholar] [CrossRef] [PubMed]
Samples | Xylose | Fructose | Glucose | Arabinose | Inositol | Sucrose | Glucose 6-Phosphate | Raffinose |
---|---|---|---|---|---|---|---|---|
A | 0.005 ± 0.001 a | 32.741 ± 4.674 a | 16.482 ± 4.321 a | 0.010 ± 0.003 a | 6.838 ± 1.351 a | 23.947 ± 4.761 a | 0.369 ± 0.071 a | 0.000 a |
B | 0.009 ± 0.002 b | 45.481 ± 5.341 a | 20.209 ± 3.312 a | 0.025 ± 0.006 b | 14.806 ± 2.147 b | 162.724 ± 14.751 b | 0.422 ± 0.123 a | 0.000 a |
C | 0.049± 0.016 a | 63.731 ± 6.454 b | 22.423 ± 2.261 a | 0.061 ± 0.017 c | 4.726 ± 1.314 a | 4.166 ± 1.531 c | 0.798 ± 0.241 b | 0.000 a |
D | 0.020 ± 0.045 c | 137.265 ± 8.671 c | 59.152 ± 7.251 b | 0.022 ± 0.006 b | 16.197 ± 2.765 b | 27.066 ± 5.141 a | 0.569 ± 0.156 a | 0.000 a |
E | 0.023 ± 0.052 c | 94.150 ± 9.543 d | 34.826 ± 5.432 c | 0.045 ± 0.017 d | 8.300 ± 1.475 a | 41.448 ± 4.751 d | 0.121 ± 0.047 c | 0.000 a |
F | 0.042 ± 0.047 a | 78.163 ± 7.241 d | 59.411 ± 6.423 b | 0.019 ± 0.008 b | 6.825 ± 1.417 a | 204.921 ± 23.241 e | 1.685 ± 0.491 d | 0.937 ± 0.251 a |
G | 0.014 ± 0.041 d | 69.939 ± 6.653 b | 66.181 ± 5.174 b | 0.004 ± 0.001 a | 13.357 ± 2.433 b | 185.235 ± 22.741 b | 0.566 ± 0.156 a | 3.258 ± 0.753 b |
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content. |
© 2024 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Zhou, Q.; Zhou, L.; Cai, Q. Strigolactones Might Regulate Ovule Development after Fertilization in Xanthoceras sorbifolium. Int. J. Mol. Sci. 2024, 25, 3276. https://doi.org/10.3390/ijms25063276
Zhou Q, Zhou L, Cai Q. Strigolactones Might Regulate Ovule Development after Fertilization in Xanthoceras sorbifolium. International Journal of Molecular Sciences. 2024; 25(6):3276. https://doi.org/10.3390/ijms25063276
Chicago/Turabian StyleZhou, Qingyuan, Linyi Zhou, and Qing Cai. 2024. "Strigolactones Might Regulate Ovule Development after Fertilization in Xanthoceras sorbifolium" International Journal of Molecular Sciences 25, no. 6: 3276. https://doi.org/10.3390/ijms25063276