The kinase and FATC domains of VvTOR affect sugar-related gene expression and sugar accumulation in grape (Vitis vinifera)
Ying Zhao
A and Xiu-Qin Wang A *
+ Author Affiliations
- Author Affiliations
A College of Food Science and Nutritional Engineering, China Agricultural University, Beijing 100083, P.R. China.
Functional Plant Biology 49(11) 927-935 https://doi.org/10.1071/FP21302
Submitted: 11 October 2021 Accepted: 23 June 2022 Published: 12 July 2022
© 2022 The Author(s) (or their employer(s)). Published by CSIRO Publishing
Abstract
The TOR (target of rapamycin) signalling network plays a pivotal role in sugar metabolism and plant growth. In this study, we used grape (Vitis vinifera L.) calli to explore the function of the kinase and FATC domains (C-terminal of FAT (FRAP-ATM-TTRAP) of VvTOR (Vitis vinifera target of rapamycin). We found that the activity of VvTOR affected sugar-related gene expression. VvTOR-VvS6K pathway potentially participated in regulating sugar gene expression. We obtained the over-expression of kinase and FATC domains in transgenic calli by Agrobacterium-mediated transformation. Even though the kinase and FATC domains all belong to VvTOR protein, their functions were different in the regulating sugar accumulation and sugar-related gene expression. We speculated that the kinase domain positively regulated sugar accumulation and FATC domain may negatively influenced sugar accumulation. FATC and kinase domains of VvTOR co-regulated sugar accumulation in grape. These observations will provide framework for future investigations to address other functions of TOR signalling in plant development and signalling pathways.
Keywords: FATC domain, grape, kinase domain, sugar accumulation, sugar-related gene expression, target of rapamycin, transgenic grape calli, VvTOR.
References
Aramburu J, Ortells MC, Tejedor S, Buxadé M, López-Rodríguez C (2014) Transcriptional regulation of the stress response by mTOR. Science Signaling 7, re2| Transcriptional regulation of the stress response by mTOR.Crossref | GoogleScholarGoogle Scholar | 24985347PubMed |
Baena-Gonzalez E, Rolland F, Thevelein JM, Sheen J (2007) A central integrator of transcription networks in plant stress and energy signalling. Nature 448, 938–942.
| A central integrator of transcription networks in plant stress and energy signalling.Crossref | GoogleScholarGoogle Scholar | 17671505PubMed |
Brunkard JO, Xu M, Scarpin MR, Chatterjee S, Shemyakina EA, Goodman HM, Zambryski P (2020) TOR dynamically regulates plant cell–cell transport. Proceedings of the National Academy of Sciences of the United States of America 117, 5049–5058.
| TOR dynamically regulates plant cell–cell transport.Crossref | GoogleScholarGoogle Scholar | 32051250PubMed |
Burkart GM, Brandizzi F (2021) A tour of TOR complex signaling in plants. Trends in Biochemical Sciences 46, 417–428.
| A tour of TOR complex signaling in plants.Crossref | GoogleScholarGoogle Scholar | 33309324PubMed |
Cai Y, Yan J, Tu W, Deng Z, Dong W, Gao H, Xu J, Zhang N, Yin L, Meng Q, Zhang Y (2020) Expression of sucrose transporters from Vitis vinifera confer high yield and enhances drought resistance in Arabidopsis. International Journal of Molecular Sciences 21, 2624
| Expression of sucrose transporters from Vitis vinifera confer high yield and enhances drought resistance in Arabidopsis.Crossref | GoogleScholarGoogle Scholar |
Dobrenel T, Caldana C, Hanson J, Robaglia C, Vincentz M, Veit B, Meyer C (2016) TOR signaling and nutrient sensing. Annual Review of Plant Biology 67, 261–285.
| TOR signaling and nutrient sensing.Crossref | GoogleScholarGoogle Scholar | 26905651PubMed |
Dong Y, Silbermann M, Speiser A, Forieri I, Linster E, Poschet G, Allboje Samami A, Wanatabe M, Sticht C, Teleman AA, Deragon J-M, Saito K, Hell R, Wirtz M (2017) Sulfur availability regulates plant growth via glucose-TOR signaling. Nature Communications 8, 1174
| Sulfur availability regulates plant growth via glucose-TOR signaling.Crossref | GoogleScholarGoogle Scholar | 29079776PubMed |
Fu L, Liu Y, Qin G, Wu P, Zi H, Xu Z, Zhao X, Wang Y, Li Y, Yang S, Peng C, Wong CCL, Yoo S-D, Zuo Z, Liu R, Cho Y-H, Xiong Y (2021) The TOR–EIN2 axis mediates nuclear signalling to modulate plant growth. Nature 591, 288–292.
| The TOR–EIN2 axis mediates nuclear signalling to modulate plant growth.Crossref | GoogleScholarGoogle Scholar | 33658715PubMed |
González A, Hall MN (2017) Nutrient sensing and TOR signaling in yeast and mammals. The EMBO Journal 36, 397–408.
| Nutrient sensing and TOR signaling in yeast and mammals.Crossref | GoogleScholarGoogle Scholar | 28096180PubMed |
Jamsheer KM, Jindal S, Laxmi A (2019) Evolution of TOR–SnRK dynamics in green plants and its integration with phytohormone signaling networks. Journal of Experimental Botany 70, 2239–2259.
| Evolution of TOR–SnRK dynamics in green plants and its integration with phytohormone signaling networks.Crossref | GoogleScholarGoogle Scholar |
Kim Y-K, Kim S, Shin Y-j, Hur Y-S, Kim W-Y, Lee M-S, Cheon C-I, Verma DPS (2014) Ribosomal protein S6, a target of rapamycin, is involved in the regulation of rRNA genes by possible epigenetic changes in Arabidopsis. Journal of Biological Chemistry 289, 3901–3912.
| Ribosomal protein S6, a target of rapamycin, is involved in the regulation of rRNA genes by possible epigenetic changes in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 24302738PubMed |
Krejci A, Tennessen JM (2017) Metabolism in time and space – exploring the frontier of developmental biology. Development 144, 3193–3198.
| Metabolism in time and space – exploring the frontier of developmental biology.Crossref | GoogleScholarGoogle Scholar | 28928279PubMed |
Lecourieux F, Kappel C, Lecourieux D, Serrano A, Torres E, Arce-Johnson P, Delrot S (2014) An update on sugar transport and signalling in grapevine. Journal of Experimental Botany 65, 821–832.
| An update on sugar transport and signalling in grapevine.Crossref | GoogleScholarGoogle Scholar | 24323501PubMed |
Li L, Sheen J (2016) Dynamic and diverse sugar signaling. Current Opinion in Plant Biology 33, 116–125.
| Dynamic and diverse sugar signaling.Crossref | GoogleScholarGoogle Scholar | 27423125PubMed |
Loewith R, Hall MN (2011) Target of rapamycin (TOR) in nutrient signaling and growth control. Genetics 189, 1177–1201.
| Target of rapamycin (TOR) in nutrient signaling and growth control.Crossref | GoogleScholarGoogle Scholar | 22174183PubMed |
Maegawa K, Takii R, Ushimaru T, Kozaki A (2015) Evolutionary conservation of TORC1 components, TOR, Raptor, and LST8, between rice and yeast. Molecular Genetics and Genomics 290, 2019–2030.
| Evolutionary conservation of TORC1 components, TOR, Raptor, and LST8, between rice and yeast.Crossref | GoogleScholarGoogle Scholar | 25956502PubMed |
Meggio F, Deana AD, Ruzzene M, Brunati AM, Cesaro L, Guerra B, Meyer T, Mett H, Fabbro D, Furet P, Dobrowolska G, Pinna LA (1995) Different susceptibility of protein kinases to staurosporine inhibition. Kinetic studies and molecular bases for the resistance of protein kinase CK2. European Journal of Biochemistry 234, 317–322.
| Different susceptibility of protein kinases to staurosporine inhibition. Kinetic studies and molecular bases for the resistance of protein kinase CK2.Crossref | GoogleScholarGoogle Scholar | 8529658PubMed |
Montané M-H, Menand B (2013) ATP-competitive mTOR kinase inhibitors delay plant growth by triggering early differentiation of meristematic cells but no developmental patterning change. Journal of Experimental Botany 64, 4361–4374.
| ATP-competitive mTOR kinase inhibitors delay plant growth by triggering early differentiation of meristematic cells but no developmental patterning change.Crossref | GoogleScholarGoogle Scholar | 23963679PubMed |
Ren M, Qiu S, Venglat P, Xiang D, Feng L, Selvaraj G, Datla R (2011) Target of rapamycin regulates development and ribosomal RNA expression through kinase domain in Arabidopsis. Plant Physiology 155, 1367–1382.
| Target of rapamycin regulates development and ribosomal RNA expression through kinase domain in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 21266656PubMed |
Ren M, Venglat P, Qiu S, Feng L, Cao Y, Wang E, Xiang D, Wang J, Alexander D, Chalivendra S, Logan D, Mattoo A, Selvaraj G, Datla R (2012) Target of rapamycin signaling regulates metabolism, growth, and life span in Arabidopsis. The Plant Cell 24, 4850–4874.
| Target of rapamycin signaling regulates metabolism, growth, and life span in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 23275579PubMed |
Rexin D, Meyer C, Robaglia C, Veit B (2015) TOR signalling in plants. Biochemical Journal 470, 1–14.
| TOR signalling in plants.Crossref | GoogleScholarGoogle Scholar | 26251442PubMed |
Robaglia C, Thomas M, Meyer C (2012) Sensing nutrient and energy status by SnRK1 and TOR kinases. Current Opinion in Plant Biology 15, 301–307.
| Sensing nutrient and energy status by SnRK1 and TOR kinases.Crossref | GoogleScholarGoogle Scholar | 22305521PubMed |
Rosenberger CL, Chen J (2018) To grow or not to grow: TOR and SnRK2 coordinate growth and stress response in Arabidopsis. Molecular Cell 69, 3–4.
| To grow or not to grow: TOR and SnRK2 coordinate growth and stress response in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 29304332PubMed |
Sehgal SN, Baker H, Vézina C (1975) Rapamycin (AY-22,989), a new antifungal antibiotic. II. Fermentation, isolation and characterization. J Antibiot (Tokyo) 10, 727–732.
| Rapamycin (AY-22,989), a new antifungal antibiotic. II. Fermentation, isolation and characterization.Crossref | GoogleScholarGoogle Scholar |
Shi L, Wu Y, Sheen J (2018) TOR signaling in plants: conservation and innovation. Development 145, dev160887
| TOR signaling in plants: conservation and innovation.Crossref | GoogleScholarGoogle Scholar | 29986898PubMed |
Tamaoki T, Nomoto H, Takahashi I, Kato Y, Morimoto M, Tomita F (1986) Staurosporine, a potent inhibitor of phospholipid Ca++ dependent protein kinase. Biochemical and Biophysical Research Communications 135, 397–402.
| Staurosporine, a potent inhibitor of phospholipid Ca++ dependent protein kinase.Crossref | GoogleScholarGoogle Scholar | 3457562PubMed |
Van Leene J, Han C, Gadeyne A, Eeckhout D, Matthijs C, Cannoot B, De Winne N, Persiau G, Van De Slijke E, Van de Cotte B, Stes E, Van Bel M, Storme V, Impens F, Gevaert K, Vandepoele K, De Smet I, De Jaeger G (2019) Capturing the phosphorylation and protein interaction landscape of the plant TOR kinase. Nature Plants 5, 316–327.
| Capturing the phosphorylation and protein interaction landscape of the plant TOR kinase.Crossref | GoogleScholarGoogle Scholar | 30833711PubMed |
Wullschleger S, Loewith R, Hall MN (2006) TOR signaling in growth and metabolism. Cell 124, 471–484.
| TOR signaling in growth and metabolism.Crossref | GoogleScholarGoogle Scholar | 16469695PubMed |
Xiong Y, Sheen J (2012) Rapamycin and glucose-target of rapamycin (TOR) protein signaling in plants. Journal of Biological Chemistry 287, 2836–2842.
| Rapamycin and glucose-target of rapamycin (TOR) protein signaling in plants.Crossref | GoogleScholarGoogle Scholar | 22134914PubMed |
Xiong Y, Sheen J (2013) Moving beyond translation: glucose-TOR signaling in the transcriptional control of cell cycle. Cell Cycle 12, 1989–1990.
| Moving beyond translation: glucose-TOR signaling in the transcriptional control of cell cycle.Crossref | GoogleScholarGoogle Scholar | 23759578PubMed |
Xiong Y, Sheen J (2015) Novel links in the plant TOR kinase signaling network. Current Opinion in Plant Biology 28, 83–91.
| Novel links in the plant TOR kinase signaling network.Crossref | GoogleScholarGoogle Scholar | 26476687PubMed |
Xiong Y, McCormack M, Li L, Hall Q, Xiang C, Sheen J (2013) Glucose–TOR signalling reprograms the transcriptome and activates meristems. Nature 496, 181–186.
| Glucose–TOR signalling reprograms the transcriptome and activates meristems.Crossref | GoogleScholarGoogle Scholar | 23542588PubMed |
Yuan X, Xu P, Yu Y, Xiong Y (2020) Glucose-TOR signaling regulates PIN2 stability to orchestrate auxin gradient and cell expansion in Arabidopsis root. Proceedings of the National Academy of Sciences of the United States of America 117, 32223–32225.
| Glucose-TOR signaling regulates PIN2 stability to orchestrate auxin gradient and cell expansion in Arabidopsis root.Crossref | GoogleScholarGoogle Scholar | 33288701PubMed |
Zhang Z, Zhu J-Y, Roh J, Marchive C, Kim S-K, Meyer C, Sun Y, Wang W, Wang Z-Y (2016) TOR signaling promotes accumulation of BZR1 to balance growth with carbon availability in Arabidopsis. Current Biology 26, 1854–1860.
| TOR signaling promotes accumulation of BZR1 to balance growth with carbon availability in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 27345161PubMed |
Zhao Y, Wang X-Q (2020) The hot issue: TOR signalling network in plants. Functional Plant Biology 48, 1–7.
| The hot issue: TOR signalling network in plants.Crossref | GoogleScholarGoogle Scholar | 32905758PubMed |
Zhuo F, Xiong F, Deng K, Li Z, Ren M (2020) Target of rapamycin (TOR) negatively regulates ethylene signals in Arabidopsis. International Journal of Molecular Sciences 21, 2680
| Target of rapamycin (TOR) negatively regulates ethylene signals in Arabidopsis.Crossref | GoogleScholarGoogle Scholar |
