TOR coordinates cytokinin and gibberellin signals mediating development and defense.

TOR cytokinin gibberellin immunity tomato

Journal

Plant, cell & environment
ISSN: 1365-3040
Titre abrégé: Plant Cell Environ
Pays: United States
ID NLM: 9309004

Informations de publication

Date de publication:
30 Oct 2023
Historique:
revised: 15 09 2023
received: 16 05 2023
accepted: 17 10 2023
medline: 31 10 2023
pubmed: 31 10 2023
entrez: 31 10 2023
Statut: aheadofprint

Résumé

Plants constantly perceive and process environmental signals and balance between the energetic demands of growth and defense. Growth arrest upon pathogen attack was previously suggested to result from a redirection of the plants' metabolic resources towards the activation of plant defense. The energy sensor Target of Rapamycin (TOR) kinase is a conserved master coordinator of growth and development in all eukaryotes. Although TOR is positioned at the interface between development and defense, little is known about the mechanisms by which TOR may potentially regulate the relationship between these two modalities. The plant hormones cytokinin (CK) and gibberellin (GA) execute various aspects of plant development and defense. The ratio between CK and GA was reported to determine the outcome of developmental programmes. Here, investigating the interplay between TOR-mediated development and TOR-mediated defense in tomato, we found that TOR silencing resulted in rescue of several different aberrant developmental phenotypes, demonstrating that TOR is required for the execution of developmental cues. In parallel, TOR inhibition enhanced immunity in genotypes with a low CK/GA ratio but not in genotypes with a high CK/GA ratio. TOR-inhibition mediated disease resistance was found to depend on developmental status, and was abolished in strongly morphogenetic leaves, while being strongest in mature, differentiated leaves. CK repressed TOR activity, suggesting that CK-mediated immunity may rely on TOR downregulation. At the same time, TOR activity was promoted by GA, and TOR silencing reduced GA sensitivity, indicating that GA signalling requires normal TOR activity. Our results demonstrate that TOR likely acts in concert with CK and GA signalling, executing signalling cues in both defense and development. Thus, differential regulation of TOR or TOR-mediated processes could regulate the required outcome of development-defense prioritisation.

Identifiants

pubmed: 37904283
doi: 10.1111/pce.14748
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Subventions

Organisme : Israel Science Foundation
ID : 1759/20

Informations de copyright

© 2023 John Wiley & Sons Ltd.

Références

Achard, P., Cheng, H., De Grauwe, L., Decat, J., Schoutteten, H., Moritz, T. et al. (2006) Integration of plant responses to environmentally activated phytohormonal signals. Science, 311, 91-94. Available from: https://doi.org/10.1126/science.1118642
Achard, P., Renou, J.P., Berthomé, R., Harberd, N.P. & Genschik, P. (2008) Plant DELLAs restrain growth and promote survival of adversity by reducing the levels of reactive oxygen species. Current Biology, 18, 656-660. Available from: https://doi.org/10.1016/j.cub.2008.04.034
Anand, G., Leibman-Markus, M., Elkabetz, D. & Bar, M. (2021) Method for the production and purification of plant immuno-active xylanase from Trichoderma. International Journal of Molecular Sciences, 22, 4214. Available from: https://doi.org/10.3390/ijms22084214
Anderson, G.H., Veit, B. & Hanson, M.R. (2005) The Arabidopsis AtRaptor genes are essential for post-embryonic plant growth. BMC Biology, 3, 12. Available from: https://doi.org/10.1186/1741-7007-3-12
Andrés, F., Porri, A., Torti, S., Mateos, J., Romera-Branchat, M., García-Martínez, J.L. et al. (2014) Short vegetative phase reduces gibberellin biosynthesis at the Arabidopsis shoot apex to regulate the floral transition. Proceedings of the National Academy of Sciences of the United States of America, 111, 2760-2769. Available from: https://doi.org/10.1073/pnas.1409567111
Argyros, R.D., Mathews, D.E., Chiang, Y.H., Palmer, C.M., Thibault, D.M., Etheridge, N. et al. (2008) Type B response regulators of Arabidopsis play key roles in cytokinin signaling and plant development. The Plant Cell, 20, 2102-2116. Available from: https://doi.org/10.1105/tpc.108.059584
Aznar, N.R., Consolo, V.F., Salerno, G.L. & Martínez-Noël, G.M.A. (2018) TOR signaling downregulation increases resistance to the cereal killer Fusarium graminearum. Plant Signaling & Behavior, 13, e1414120. Available from: https://doi.org/10.1080/15592324.2017.1414120
Bar, M., Israeli, A., Levy, M., Ben Gera, H., Jiménez-Gómez, J.M., Kouril, S. et al. (2016) CLAUSA is a MYB transcription factor that promotes leaf differentiation by attenuating cytokinin signaling. The Plant Cell, 28, 1602-1615. Available from: https://doi.org/10.1105/tpc.16.00211
Bari, R. & Jones, J.D.G. (2009) Role of plant hormones in plant defence responses. Plant Molecular Biology, 69, 473-488. Available from: https://doi.org/10.1007/s11103-008-9435-0
Bartrina, I., Otto, E., Strnad, M., Werner, T. & Schmülling, T. (2011) Cytokinin regulates the activity of reproductive meristems, flower organ size, ovule formation, and thus seed yield in Arabidopsis thaliana. The Plant Cell, 23, 69-80. Available from: https://doi.org/10.1105/tpc.110.079079
Berens, M.L., Wolinska, K.W., Spaepen, S., Ziegler, J., Nobori, T., Nair, A. et al. (2019) Balancing trade-offs between biotic and abiotic stress responses through leaf age-dependent variation in stress hormone cross-talk. Proceedings of the National Academy of Sciences of the United States of America, 116, 2364-2373. Available from: https://doi.org/10.1073/pnas.1817233116
Berry, H.M. & Argueso, C.T. (2022) More than growth: phytohormone-regulated transcription factors controlling plant immunity, plant development and plant architecture. Current Opinion in Plant Biology, 70, 102309. Available from: https://doi.org/10.1016/j.pbi.2022.102309
Bolduc, N. & Hake, S. (2009) The maize transcription factor KNOTTED1 directly regulates the gibberellin catabolism gene ga2ox1. The Plant Cell, 21, 1647-1658. Available from: https://doi.org/10.1105/tpc.109.068221
Bonaccorso, O., Lee, J.E., Puah, L., Scutt, C.P. & Golz, J.F. (2012) FILAMENTOUS FLOWER controls lateral organ development by acting as both an activator and a repressor. BMC Plant Biology, 12, 176. Available from: https://doi.org/10.1186/1471-2229-12-176
Brenner, W.G., Romanov, G.A., Köllmer, I., Bürkle, L. & Schmülling, T. (2005) Immediate-early and delayed cytokinin response genes of Arabidopsis thaliana identified by genome-wide expression profiling reveal novel cytokinin-sensitive processes and suggest cytokinin action through transcriptional cascades. The Plant Journal, 44, 314-333. Available from: https://doi.org/10.1111/j.1365-313X.2005.02530.x
Brenner, W.G. & Schmülling, T. (2012) Transcript profiling of cytokinin action in Arabidopsis roots and shoots discovers largely similar but also organ-specific responses. BMC Plant Biology, 12, 112. Available from: https://doi.org/10.1186/1471-2229-12-112
Brunkard, J.O., Xu, M., Scarpin, M.R., Chatterjee, S., Shemyakina, E.A., Goodman, H.M. et al. (2020) TOR dynamically regulates plant cell-cell transport. Proceedings of the National Academy of Sciences of the United States of America, 117, 5049-5058. Available from: https://doi.org/10.1073/pnas.1919196117
De Bruyne, L., Höfte, M. & De Vleesschauwer, D. (2014) Connecting growth and defense: the emerging roles of brassinosteroids and gibberellins in plant innate immunity. Molecular Plant, 7, 943-959. Available from: https://doi.org/10.1093/mp/ssu050
Busch, B.L., Schmitz, G., Rossmann, S., Piron, F., Ding, J., Bendahmane, A. et al. (2011) Shoot branching and leaf dissection in tomato are regulated by homologous gene modules. The Plant Cell, 23, 3595-3609. Available from: https://doi.org/10.1105/tpc.111.087981
Caldana, C., Li, Y., Leisse, A., Zhang, Y., Bartholomaeus, L., Fernie, A.R. et al. (2013) Systemic analysis of inducible target of rapamycin mutants reveal a general metabolic switch controlling growth in Arabidopsis thaliana. The Plant Journal, 73, 897-909. Available from: https://doi.org/10.1111/tpj.12080
Caldana, C., Martins, M.C.M., Mubeen, U. & Urrea-Castellanos, R. (2019) The magic ‘hammer’ of TOR: the multiple faces of a single pathway in the metabolic regulation of plant growth and development. Journal of Experimental Botany, 70, 2217-2225. Available from: https://doi.org/10.1093/jxb/ery459
Campos, M.L., Yoshida, Y., Major, I.T., De Oliveira Ferreira, D., Weraduwage, S.M., Froehlich, J.E. et al. (2016) Rewiring of jasmonate and phytochrome B signalling uncouples plant growth-defense tradeoffs. Nature Communications, 7, 12570. Available from: https://doi.org/10.1038/ncomms12570
Cao, P., Kim, S.J., Xing, A., Schenck, C.A., Liu, L. & Jiang, N. et al. (2019) Homeostasis of branched-chain amino acids is critical for the activity of TOR signaling in Arabidopsis. eLife, 8, 50747. Available from: https://doi.org/10.7554/eLife.50747
Černý, M., Kuklová, A., Hoehenwarter, W., Fragner, L., Novák, O., Rotková, G. et al. (2013) Proteome and metabolome profiling of cytokinin action in Arabidopsis identifying both distinct and similar responses to cytokinin down- and up-regulation. Journal of Experimental Botany, 64, 4193-4206. Available from: https://doi.org/10.1093/jxb/ert227
Choi, J., Huh, S.U., Kojima, M., Sakakibara, H., Paek, K.H. & Hwang, I. (2010) The cytokinin-activated transcription factor ARR2 promotes plant immunity via TGA3/NPR1-dependent salicylic acid signaling in arabidopsis. Developmental Cell, 19, 284-295. Available from: https://doi.org/10.1016/j.devcel.2010.07.011
Colebrook, E.H., Thomas, S.G., Phillips, A.L. & Hedden, P. (2014) The role of gibberellin signalling in plant responses to abiotic stress. Journal of Experimental Biology, 217, 67-75. Available from: https://doi.org/10.1242/jeb.089938
Davière, J.M. & Achard, P. (2013) Gibberellin signaling in plants. Development, 140, 1147-1151. Available from: https://doi.org/10.1242/dev.087650
Deprost, D., Yao, L., Sormani, R., Moreau, M., Leterreux, G. & Nicolaï, M. et al. (2007) The Arabidopsis TOR kinase links plant growth, yield, stress resistance and mRNA translation. EMBO Reports, 8, 864-870. Available from: https://doi.org/10.1038/sj.embor.7401043
Develey-Rivière, M.P. & Galiana, E. (2007) Resistance to pathogens and host developmental stage: a multifaceted relationship within the plant kingdom. New Phytologist, 175, 405-416. Available from: https://doi.org/10.1111/j.1469-8137.2007.02130.x
Dobrenel, T., Caldana, C., Hanson, J., Robaglia, C., Vincentz, M., Veit, B. et al. (2016) TOR signaling and nutrient sensing. Annual Review of Plant Biology, 67, 261-285. Available from: https://doi.org/10.1146/annurev-arplant-043014-114648
Dong, P., Xiong, F., Que, Y., Wang, K., Yu, L., Li, Z. et al. (2015) Expression profiling and functional analysis reveals that TOR is a key player in regulating photosynthesis and phytohormone signaling pathways in Arabidopsis. Frontiers in Plant Science, 6, 1-15. Available from: https://doi.org/10.3389/fpls.2015.00677
Du, F., Guan, C. & Jiao, Y. (2018) Molecular mechanisms of leaf morphogenesis. Molecular Plant, 11, 1117-1134. Available from: https://doi.org/10.1016/j.molp.2018.06.006
Efroni, I., Han, S.K., Kim, H.J., Wu, M.F., Steiner, E., Birnbaum, K.D. et al. (2013) Regulation of leaf maturation by chromatin-mediated modulation of cytokinin responses. Developmental Cell, 24, 438-445. Available from: https://doi.org/10.1016/j.devcel.2013.01.019
Eichmann, R. & Schäfer, P. (2015) Growth versus immunity-a redirection of the cell cycle? Current Opinion in Plant Biology, 26, 106-112. Available from: https://doi.org/10.1016/j.pbi.2015.06.006
Ezura, H. & Harberd, N. (1995) Endogenous gibberellin levels influence in-vitro shoot regeneration in Arabidopsis thaliana (L.) Heynh. Planta, 197, 301-305. Available from: https://doi.org/10.1007/BF00202651
Farber, M., Attia, Z. & Weiss, D. (2016) Cytokinin activity increases stomatal density and transpiration rate in tomato. Journal of Experimental Botany, 67, 6351-6362. Available from: https://doi.org/10.1093/jxb/erw398
Fleishon, S., Shani, E., Ori, N. & Weiss, D. (2011) Negative reciprocal interactions between gibberellin and cytokinin in tomato. New Phytologist, 190, 609-617. Available from: https://doi.org/10.1111/j.1469-8137.2010.03616.x
George Jones, M. (1987) Gibberellins and the procera mutant of tomato. Planta, 172, 280-284. Available from: https://doi.org/10.1007/bf00394598
Goss, E.M. & Bergelson, J. (2006) Variation in resistance and virulence in the interaction between Arabidopsis thaliana and a bacterial pathogen. Evolution; International Journal of Organic Evolution, 60, 1562-1573. Available from: https://doi.org/10.1554/06-200.1
Greenboim-Wainberg, Y., Maymon, I., Borochov, R., Alvarez, J., Olszewski, N., Ori, N. et al. (2005) Cross talk between gibberellin and cytokinin: the Arabidopsis GA response inhibitor SPINDLY plays a positive role in cytokinin signaling. The Plant Cell, 17, 92-102. Available from: https://doi.org/10.1105/tpc.104.028472
Großkinsky, D.K., Naseem, M., Abdelmohsen, U.R., Plickert, N., Engelke, T., Griebel, T. et al. (2011) Cytokinins mediate resistance against Pseudomonas syringae in tobacco through increased antimicrobial phytoalexin synthesis independent of salicylic acid signaling. Plant Physiology, 157, 815-830. Available from: https://doi.org/10.1104/pp.111.182931
Gupta, R., Anand, G., Pizarro, L., Laor, D., Kovetz, N., Sela, N. et al. (2021a) Cytokinin inhibits fungal development and virulence by targeting the cytoskeleton and cellular trafficking. mBio, 12, 1-22. Available from: https://doi.org/10.1128/mBio.03068-20
Gupta, R., Elkabetz, D., Leibman-Markus, M., Jami, E. & Bar, M. (2022) Cytokinin-microbiome interactions regulate developmental functions. Environmental microbiome, 17, 2. Available from: https://doi.org/10.1186/s40793-022-00397-2
Gupta, R., Leibman-Markus, M., Pizarro, L. & Bar, M. (2021b) Cytokinin induces bacterial pathogen resistance in tomato. Plant Pathology, 70, 318-325. Available from: https://doi.org/10.1111/ppa.13279
Gupta, R., Pizarro, L., Leibman-Markus, M., Marash, I. & Bar, M. (2020) Cytokinin response induces immunity and fungal pathogen resistance, and modulates trafficking of the PRR LeEIX2 in tomato. Molecular Plant Pathology, 21, 1287-1306. Available from: https://doi.org/10.1111/mpp.12978
Harberd, N.P., Belfield, E. & Yasumura, Y. (2009) The angiosperm gibberellin-GID1-DELLA growth regulatory mechanism: how an “inhibitor of an inhibitor” enables flexible response to fluctuating environments. The Plant Cell, 21, 1328-1339. Available from: https://doi.org/10.1105/tpc.109.066969
Hauvermale, A.L., Ariizumi, T. & Steber, C.M. (2012) Gibberellin signaling: a theme and variations on DELLA repression. Plant Physiology, 160, 83-92. Available from: https://doi.org/10.1104/pp.112.200956
Hay, A., Kaur, H., Phillips, A., Hedden, P., Hake, S., Tsiantis, M. et al. (2005) The gibberellin pathway mediates KNOTTED1-type homeobox function in plants with different body plans. Current Biology, 12, 1566-1571. Available from: https://doi.org/10.1016/j.cub.2005.07.060
Hay, A. & Tsiantis, M. (2010) KNOX genes: versatile regulators of plant development and diversity. Development, 137, 3153-3165. Available from: https://doi.org/10.1242/dev.030049
Hedden, P. (2020) The current status of research on gibberellin biosynthesis. Plant and Cell Physiology, 61, 1832-1849. Available from: https://doi.org/10.1093/pcp/pcaa092
Horiguchi, G., Mollá-Morales, A., Pérez-Pérez, J.M., Kojima, K., Robles, P., Ponce, M.R. et al. (2011) Differential contributions of ribosomal protein genes to Arabidopsis thaliana leaf development. The Plant Journal, 65, 724-736. Available from: https://doi.org/10.1111/j.1365-313X.2010.04457.x
Ishida, K., Yamashino, T., Yokoyama, A. & Mizuno, T. (2008) Three type-B response regulators, ARR1, ARR10 and ARR12, play essential but redundant roles in cytokinin signal transduction throughout the life cycle of Arabidopsis thaliana. Plant and Cell Physiology, 49, 47-57. Available from: https://doi.org/10.1093/pcp/pcm165
Israeli, A., Burko, Y., Shleizer-Burko, S., Zelnik, I.D., Sela, N., Hajirezaei, M.R. et al. (2021) Coordinating the morphogenesis-differentiation balance by tweaking the cytokinin-gibberellin equilibrium. PLoS Genetics, 17, e1009537. Available from: https://doi.org/10.1371/journal.pgen.1009537
Israeli, A., Capua, Y., Shwartz, I., Tal, L., Meir, Z., Levy, M. et al. (2019) Multiple auxin-response regulators enable stability and variability in leaf development. Current Biology, 29, 1746-1759.e5. Available from: https://doi.org/10.1016/j.cub.2019.04.047
Jacob, D., David, D.R., Sztjenberg, A. & Elad, Y. (2008) Conditions for development of powdery mildew of tomato caused by Oidium neolycopersici. Phytopathology, 98, 270-281. Available from: https://doi.org/10.1094/PHYTO-98-3-0270
Jasinski, S., Piazza, P., Craft, J., Hay, A., Woolley, L., Rieu, I. et al. (2005) KNOX action in Arabidopsis is mediated by coordinate regulation of cytokinin and gibberellin activities. Current Biology, 15, 1560-1565. Available from: https://doi.org/10.1016/j.cub.2005.07.023
Jasinski, S., Tattersall, A., Piazza, P., Hay, A., Martinez-garcia, J.F., Schmitz, G. et al. (2008) PROCERA encodes a DELLA protein that mediates control of dissected leaf form in tomato. The Plant Journal: For Cell and Molecular Biology, 56, 603-612. Available from: https://doi.org/10.1111/j.1365-313X.2008.03628.x
Jiang, C., Fan, Z., Li, Z., Niu, D., Li, Y., Zheng, M. et al. (2020) Bacillus cereus AR156 triggers induced systemic resistance against Pseudomonas syringae pv. tomato DC3000 by suppressing miR472 and activating CNLs-mediated basal immunity in Arabidopsis. Molecular Plant Pathology, 21, 854-870. Available from: https://doi.org/10.1111/mpp.12935
Jiang, C.J., Shimono, M., Sugano, S., Kojima, M., Liu, X., Inoue, H. et al. (2013) Cytokinins act synergistically with salicylic acid to activate defense gene expression in rice. Molecular Plant-Microbe Interactions®, 26, 287-296. Available from: https://doi.org/10.1094/MPMI-06-12-0152-R
Kakimoto, T. (2001) Identification of plant cytokinin biosynthetic enzymes as dimethylallyl diphosphate:ATP/ADP isopentenyltransferases. Plant and Cell Physiology, 42, 677-685. Available from: https://doi.org/10.1093/pcp/pce112
Karasov, T.L., Chae, E., Herman, J.J. & Bergelson, J. (2017) Mechanisms to mitigate the trade-off between growth and defense. The Plant Cell, 29, 666-680. Available from: https://doi.org/10.1105/tpc.16.00931
Kimura, S., Koenig, D., Kang, J., Yoong, F.Y. & Sinha, N. (2008) Natural variation in leaf morphology results from mutation of a novel KNOX gene. Current Biology, 18, 672-677. Available from: https://doi.org/10.1016/j.cub.2008.04.008
Kliebenstein, D.J. (2016) False idolatry of the mythical growth versus immunity tradeoff in molecular systems plant pathology. Physiological and Molecular Plant Pathology, 95, 55-59. Available from: https://doi.org/10.1016/j.pmpp.2016.02.004
Kurakawa, T., Ueda, N., Maekawa, M., Kobayashi, K., Kojima, M., Nagato, Y. et al. (2007) Direct control of shoot meristem activity by a cytokinin-activating enzyme. Nature, 445, 652-655. Available from: https://doi.org/10.1038/nature05504
Kuroha, T., Tokunaga, H., Kojima, M., Ueda, N., Ishida, T., Nagawa, S. et al. (2009) Functional analyses of LONELY GUY cytokinin-activating enzymes reveal the importance of the direct activation pathway in Arabidopsis. The Plant Cell, 21, 3152-3169. Available from: https://doi.org/10.1105/tpc.109.068676
Leibman-Markus, M., Schuster, S. & Avni, A. (2017) LeEIX2 interactors' analysis and EIX-mediated responses measurement. Methods in Molecular Biology, 1578, 167-172. Available from: https://doi.org/10.1007/978-1-4939-6859-6_13.
Li, X., Cai, W., Liu, Y., Li, H., Fu, L., Liu, Z. et al. (2017) Differential TOR activation and cell proliferation in Arabidopsis root and shoot apexes. Proceedings of the National Academy of Sciences of the United States of America, 114, 2765-2770. Available from: https://doi.org/10.1073/pnas.1618782114
Lifschitz, E., Eviatar, T., Rozman, A., Shalit, A., Goldshmidt, A., Amsellem, Z. et al. (2006) The tomato FT ortholog triggers systemic signals that regulate growth and flowering and substitute for diverse environmental stimuli. Proceedings of the National Academy of Sciences of the United States of America, 103, 6398-6403. Available from: https://doi.org/10.1073/pnas.0601620103
Liu, Y. & Bassham, D.C. (2010) TOR is a negative regulator of autophagy in Arabidopsis thaliana. PLoS One, 5, 11883. Available from: https://doi.org/10.1371/journal.pone.0011883
Liu, Y., Duan, X., Zhao, X., Ding, W., Wang, Y. & Xiong, Y. (2021) Diverse nitrogen signals activate convergent ROP2-TOR signaling in Arabidopsis. Developmental Cell, 56, 1283-1295.e5. Available from: https://doi.org/10.1016/j.devcel.2021.03.022
Liu, Y., Schiff, M. & Dinesh-Kumar, S.P. (2002) Virus-induced gene silencing in tomato. The Plant Journal, 31, 777-786. Available from: https://doi.org/10.1046/j.1365-313X.2002.01394.x
Livne, S., Lor, V.S., Nir, I., Eliaz, N., Aharoni, A., Olszewski, N.E. et al. (2015) Uncovering DELLA-independent gibberellin responses by characterizing new tomato procera mutants. The Plant Cell, 27, 1579-1594. Available from: https://doi.org/10.1105/tpc.114.132795
Locascio, A., Blázquez, M.A. & Alabadí, D. (2013) Genomic analysis of della protein activity. Plant and Cell Physiology, 54, 1229-1237. Available from: https://doi.org/10.1093/pcp/pct082
Major, I.T., Guo, Q., Zhai, J., Kapali, G., Kramer, D.M. & Howe, G.A. (2020) A phytochrome b-independent pathway restricts growth at high levels of jasmonate defense. Plant Physiology, 183, 733-749. Available from: https://doi.org/10.1104/pp.19.01335
Mao, Y.B., Liu, Y.Q., Chen, D.Y., Chen, F.Y., Fang, X., Hong, G.J. et al. (2017) Jasmonate response decay and defense metabolite accumulation contributes to age-regulated dynamics of plant insect resistance. Nature Communications, 8, 13925. Available from: https://doi.org/10.1038/ncomms13925
Marash, I., Leibman-Markus, M., Gupta, R., Avni, A. & Bar, M. (2022) TOR inhibition primes immunity and pathogen resistance in tomato in a salicylic acid-dependent manner. Molecular Plant Pathology, 23, 1035-1047. Available from: https://doi.org/10.1111/mpp.13207
Margalha, L., Confraria, A. & Baena-González, E. (2019) SnRK1 and TOR: modulating growth-defense trade-offs in plant stress responses. Journal of Experimental Botany, 70, 2261-2274. Available from: https://doi.org/10.1093/jxb/erz066
Márquez-López, R.E., Quintana-Escobar, A.O. & Loyola-Vargas, V.M. (2019) Cytokinins, the Cinderella of plant growth regulators. Phytochemistry Reviews, 18, 1387-1408. Available from: https://doi.org/10.1007/s11101-019-09656-6
McCready, K., Spencer, V. & Kim, M. (2020) The importance of TOR kinase in plant development. Frontiers in Plant Science, 11, 1-7. Available from: https://doi.org/10.3389/fpls.2020.00016
Meldau, S., Erb, M. & Baldwin, I.T. (2012) Defence on demand: mechanisms behind optimal defence patterns. Annals of Botany, 110, 1503-1514. Available from: https://doi.org/10.1093/aob/mcs212
Meteignier, L.V., El Oirdi, M., Cohen, M., Barff, T., Matteau, D. & Lucier, J.F. et al. (2018) Corrigendum: translatome analysis of an NB-LRR immune response identifies important contributors to plant immunity in Arabidopsis (Journal of Experimental Botany (2017) 68:9 (2333-2344). Journal of Experimental Botany, 69, 3785. Available from: https://doi.org/10.1093/jxb/erx078
Mok, D.W.S. & Mok, M.C. (2001) Etabolism and. Perception, 52, 89-118.
Monson, R.K., Trowbridge, A.M., Lindroth, R.L. & Lerdau, M.T. (2022) Coordinated resource allocation to plant growth-defense tradeoffs. New Phytologist, 233, 1051-1066. Available from: https://doi.org/10.1111/nph.17773
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. Available from: https://doi.org/10.1093/jxb/ert242
Moreau, M., Azzopardi, M., Clé ment, G., Dobrenel, T., Marchive, C., Renne, C. et al. (2012) Mutations in the arabidopsis homolog of LST8/GβL, a partner of the target of rapamycin kinase, impair plant growth, flowering, and metabolic adaptation to long days. The Plant Cell, 24, 463-481. Available from: https://doi.org/10.1105/tpc.111.091306
Moss, W.P., Byrne, J.M., Campbell, H.L., Ji, P., Bonas, U., Jones, J.B. et al. (2007) Biological control of bacterial spot of tomato using hrp mutants of Xanthomonas campestris pv. vesicatoria. Biological Control, 41, 199-206. Available from: https://doi.org/10.1016/j.biocontrol.2007.01.008
Murase, K., Hirano, Y., Sun, T. & Hakoshima, T. (2008) Gibberellin-induced DELLA recognition by the gibberellin receptor GID1. Nature, 456, 459-463. Available from: https://doi.org/10.1038/nature07519
Nakayama, H., Rowland, S.D., Cheng, Z., Zumstein, K., Kang, J., Kondo, Y. et al. (2021) Leaf form diversification in an ornamental heirloom tomato results from alterations in two different HOMEOBOX genes. Current Biology, 31, 4788-4799.e5. Available from: https://doi.org/10.1016/j.cub.2021.08.023
Naseem, M., Philippi, N., Hussain, A., Wangorsch, G., Ahmed, N. & Dandekar, T. (2012) Integrated systems view on networking by hormones in Arabidopsis immunity reveals multiple crosstalk for cytokinin. The Plant Cell, 24, 1793-1814. Available from: https://doi.org/10.1105/tpc.112.098335
Navarro, L., Bari, R., Achard, P., Lisón, P., Nemri, A., Harberd, N.P. et al. (2008) DELLAs control plant immune responses by modulating the balance of jasmonic acid and salicylic acid signaling. Current Biology, 18, 650-655. Available from: https://doi.org/10.1016/j.cub.2008.03.060
Nelissen, H., Rymen, B., Jikumaru, Y., Demuynck, K., Van Lijsebettens, M., Kamiya, Y. et al. (2012) A local maximum in gibberellin levels regulates maize leaf growth by spatial control of cell division. Current Biology, 22, 1183-1187. Available from: https://doi.org/10.1016/j.cub.2012.04.065
Nir, I., Shohat, H., Panizel, I., Olszewski, N., Aharoni, A. & Weiss, D. (2017) The tomato DELLA protein PROCERA acts in guard cells to promote stomatal closure. The Plant Cell, 29, 3186-3197. Available from: https://doi.org/10.1105/tpc.17.00542
Nishiyama, R., Watanabe, Y., Fujita, Y., Le, D.T., Kojima, M., Werner, T. et al. (2011) Analysis of cytokinin mutants and regulation of cytokinin metabolic genes reveals important regulatory roles of cytokinins in drought, salt and abscisic acid responses, and abscisic acid biosynthesis. The Plant Cell, 23, 2169-2183. Available from: https://doi.org/10.1105/tpc.111.087395
Ori, N., Cohen, A.R., Etzioni, A., Brand, A., Yanai, O., Shleizer, S. et al. (2007) Regulation of LANCEOLATE by miR319 is required for compound-leaf development in tomato. Nature Genetics, 39, 787-791. Available from: https://doi.org/10.1038/ng2036
Pereyra, C.M., Aznar, N.R., Rodriguez, M.S., Salerno, G.L. & Martínez-Noël, G.M.A. (2020) Target of rapamycin signaling is tightly and differently regulated in the plant response under distinct abiotic stresses. Planta, 251, 21. Available from: https://doi.org/10.1007/s00425-019-03305-0
Pizarro, L., Leibman-Markus, M., Schuster, S., Bar, M., Meltz, T. & Avni, A. (2018) Tomato prenylated RAB acceptor protein 1 modulates trafficking and degradation of the pattern recognition receptor LeEIX2, affecting the innate immune response. Frontiers in Plant Science, 9, 257. Available from: https://doi.org/10.3389/fpls.2018.00257
Qin, X., Liu, J.H., Zhao, W.S., Chen, X.J., Guo, Z.J. & Peng, Y.L. (2013) Gibberellin 20-oxidase gene OsGA20ox3 regulates plant stature and disease development in rice. Molecular Plant-Microbe Interactions®, 26, 227-239. Available from: https://doi.org/10.1094/MPMI-05-12-0138-R
Redig, P., Schmulling, T. & Van Onckelen, H. (1996) Analysis of cytokinin metabolism in ipt transgenic tobacco by liquid chromatography-tandem mass spectrometry. Plant Physiology, 112, 141-148. Available from: https://doi.org/10.1104/pp.112.1.141
Reid, D.E., Heckmann, A.B., Novák, O., Kelly, S. & Stougaard, J. (2016) Cytokinin oxidase/dehydrogenase3 maintains cytokinin homeostasis during root and nodule development in Lotus japonicus. Plant Physiology, 170, 1060-1074. Available from: https://doi.org/10.1104/pp.15.00650
Ryabova, L.A., Robaglia, C. & Meyer, C. (2019) Target of rapamycin kinase: central regulatory hub for plant growth and metabolism. Journal of Experimental Botany, 70, 2211-2216. Available from: https://doi.org/10.1093/jxb/erz108
Sakamoto, T., Kamiya, N., Ueguchi-Tanaka, M., Iwahori, S. & Matsuoka, M. (2001) KNOX homeodomain protein directly suppresses the expression of a gibberellin biosynthetic gene in the tobacco shoot apical meristem. Genes & Development, 15, 581-590. Available from: https://doi.org/10.1101/gad.867901
Sakamoto, T., Sakakibara, H., Kojima, M., Yamamoto, Y., Nagasaki, H., Inukai, Y. et al. (2006) Ectopic expression of KNOTTED1-like homeobox protein induces expression of cytokinin biosynthesis genes in rice. Plant Physiology, 142, 54-62. Available from: https://doi.org/10.1104/pp.106.085811
Saxton, R.A. & Sabatini, D.M. (2017) mTOR signaling in growth, metabolism, and disease. Cell, 168, 960-976. Available from: https://doi.org/10.1016/j.cell.2017.02.004
Shani, E., Ben-Gera, H., Shleizer-Burko, S., Burko, Y., Weiss, D. & Ori, N. (2010) Cytokinin regulates compound leaf development in tomato. The Plant Cell, 22, 3206-3217. Available from: https://doi.org/10.1105/tpc.110.078253
Shani, E., Yanai, O. & Ori, N. (2006) The role of hormones in shoot apical meristem function. Current Opinion in Plant Biology, 9, 484-489. Available from: https://doi.org/10.1016/j.pbi.2006.07.008
Shi, L. & Olszewski, N.E. (1998) Gibberellin and abscisic acid regulate GAST1 expression at the level of transcription. Plant Molecular Biology, 38, 1053-1060. Available from: https://doi.org/10.1023/A:1006007315718
Shi, L., Wu, Y. & Sheen, J. (2018) TOR signaling in plants: conservation and innovation. Development, 145, dev160887. Available from: https://doi.org/10.1242/dev.160887
Shleizer-Burko, S., Burko, Y., Ben-Herzel, O. & Ori, N. (2011) Dynamic growth program regulated by LANCEOLATE enables flexible leaf patterning. Development, 138, 695-704. Available from: [pii] https://doi.org/10.1242/dev.056770
Shwartz, I., Levy, M., Ori, N. & Bar, M. (2016) Hormones in tomato leaf development. Developmental Biology, 419, 132-142. Available from: https://doi.org/10.1016/j.ydbio.2016.06.023
Smailov, B., Alybayev, S., Smekenov, I., Mursalimov, A., Saparbaev, M., Sarbassov, D. et al. (2020) Wheat germination is dependent on plant target of rapamycin signaling. Frontiers in Cell and Developmental Biology, 8, 6060685. Available from: https://doi.org/10.3389/fcell.2020.606685
Smigocki, A., Neal, J.W., McCanna, I. & Douglass, L. (1993) Cytokinin-mediated insect resistance in nicotiana plants transformed with the ipt gene. Plant Molecular Biology, 23, 325-335. Available from: https://doi.org/10.1007/BF00029008
Smigocki, A.C. & Owens, L.D. (1988) Cytokinin gene fused with a strong promoter enhances shoot organogenesis and zeatin levels in transformed plant cells. Proceedings of the National Academy of Sciences, 85, 5131-5135. Available from: https://doi.org/10.1073/pnas.85.14.5131
Song, L., Xu, G., Li, T., Zhou, H., Lin, Q., Chen, J. et al. (2022) The RALF1-FERONIA complex interacts with and activates TOR signaling in response to low nutrients. Molecular Plant, 15, 1120-1136. Available from: https://doi.org/10.1016/j.molp.2022.05.004
Song, Y., Zhao, G., Zhang, X., Li, L., Xiong, F., Zhuo, F. et al. (2017) The crosstalk between target of rapamycin (TOR) and jasmonic acid (JA) signaling existing in Arabidopsis and cotton. Scientific Reports, 7, 1-15. Available from: https://doi.org/10.1038/srep45830
Soprano, A.S., Smetana, J.H.C. & Benedetti, C.E. (2018) Regulation of tRNA biogenesis in plants and its link to plant growth and response to pathogens. Biochimica et Biophysica Acta (BBA) - Gene Regulatory Mechanisms, 1861, 344-353. Available from: https://doi.org/10.1016/j.bbagrm.2017.12.004
Steiner, E., Israeli, A., Gupta, R., Shwartz, I., Nir, I., Leibman-Markus, M. et al. (2020) Characterization of the cytokinin sensor TCSv2 in arabidopsis and tomato. Plant Methods, 16, 152. Available from: https://doi.org/10.1186/s13007-020-00694-2
Steiner, E., Livne, S., Kobinson-Katz, T., Tal, L., Pri-Tal, O., Mosquna, A. et al. (2016) The putative O-linked N-acetylglucosamine transferase SPINDLY inhibits class I TCP proteolysis to promote sensitivity to cytokinin. Plant Physiology, 171, 1485-1494. Available from: https://doi.org/10.1104/pp.16.00343
Sun, T. (2010) Gibberellin-GID1-DELLA: A pivotal regulatory module for plant growth and development. Plant Physiology, 154, 567-570. Available from: https://doi.org/10.1104/pp.110.161554
Sun, X., Jones, W.T. & Rikkerink, E.H.A. (2012) GRAS proteins: the versatile roles of intrinsically disordered proteins in plant signalling. Biochemical Journal, 442, 1-12. Available from: https://doi.org/10.1042/BJ20111766
Takei, K., Sakakibara, H. & Sugiyama, T. (2001) Identification of genes encoding adenylate isopentenyltransferase, a cytokinin biosynthesis enzyme, in Arabidopsis thaliana. Journal of Biological Chemistry, 276, 26405-26410. Available from: https://doi.org/10.1074/jbc.M102130200
Teper, D., Girija, A.M., Bosis, E., Popov, G., Savidor, A. & Sessa, G. (2018) The xanthomonas euvesicatoria type III effector XopAU is an active protein kinase that manipulates plant MAP kinase signaling. PLoS Pathogens, 14, e1006880. Available from: https://doi.org/10.1371/journal.ppat.1006880
Turck, F., Zilbermann, F., Kozma, S.C., Thomas, G. & Nagy, F. (2004) Phytohormones participate in an S6 kinase signal transduction pathway in arabidopsis. Plant Physiology, 134, 1527-1535. Available from: https://doi.org/10.1104/pp.103.035873
Upadhyaya, S., Agrawal, S., Gorakshakar, A. & Rao, B.J. (2020) TOR kinase activity in Chlamydomonas reinhardtii is modulated by cellular metabolic states. FEBS Letters, 594, 3122-3141. Available from: https://doi.org/10.1002/1873-3468.13888
Vercruyssen, L., Gonzalez, N., Werner, T., Schmülling, T. & Inzé, D. (2011) Combining enhanced root and shoot growth reveals cross talk between pathways that control plant organ size in arabidopsis. Plant Physiology, 155, 1339-1352. Available from: https://doi.org/10.1104/pp.110.167049
de Vleesschauwer, D., van Buyten, E., Satoh, K., Balidion, J., Mauleon, R., Choi, I.R. et al. (2012) Brassinosteroids antagonize gibberellin- and salicylate-mediated root immunity in rice. Plant Physiology, 158, 1833-1846. Available from: https://doi.org/10.1104/pp.112.193672
de Vleesschauwer, D., Filipe, O., Hoffman, G., Seifi, H.S., Haeck, A., Canlas, P. et al. (2018) Target of rapamycin signaling orchestrates growth-defense trade-offs in plants. New Phytologist, 217, 305-319. Available from: https://doi.org/10.1111/nph.14785
de Vleesschauwer, D., Seifi, H.S., Filipe, O., Haeck, A., Huu, S.N., Demeestere, K. et al. (2016) The DELLA protein SLR1 integrates and amplifies salicylic acid- and jasmonic acid-dependent innate immunity in rice. Plant Physiology, 170, 1831-1847. Available from: https://doi.org/10.1104/pp.15.01515
Wang, P., Zhao, Y., Li, Z., Hsu, C.C., Liu, X., Fu, L. et al. (2018) Reciprocal regulation of the TOR kinase and ABA receptor balances plant growth and stress response. Molecular Cell, 69, 100-112.e6. Available from: https://doi.org/10.1016/j.molcel.2017.12.002
Wang, X., Han, F., Yang, M., Yang, P. & Shen, S. (2013) Exploring the response of rice (Oryza sativa) leaf to gibberellins: A proteomic strategy. Rice, 6, 17. Available from: https://doi.org/10.1186/1939-8433-6-17
Weiss, D. & Ori, N. (2007) Mechanisms of cross talk between gibberellin and other hormones. Plant Physiology, 144, 1240-1246. Available from: https://doi.org/10.1104/pp.107.100370
Werner, T., Köllmer, I., Bartrina, I., Holst, K. & Schmülling, T. (2006) New insights into the biology of cytokinin degradation. Plant Biology, 8, 371-381. Available from: https://doi.org/10.1055/s-2006-923928
Werner, T., Motyka, V., Laucou, V., Smets, R., Van Onckelen, H. & Schmülling, T. (2003) Cytokinin-deficient transgenic Arabidopsis plants show multiple developmental alterations indicating opposite functions of cytokinins in the regulation of shoot and root meristem activity. The Plant Cell, 15, 2532-2550. Available from: https://doi.org/10.1105/tpc.014928
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. Available from: https://doi.org/10.1038/nature12030
Xiong, Y. & Sheen, J. (2012) Rapamycin and glucose-target of rapamycin (TOR) protein signaling in plants. Journal of Biological Chemistry, 287, 2836-2842. Available from: https://doi.org/10.1074/jbc.M111.300749
Xu, Y.P., Lv, L.H., Xu, Y.J., Yang, J., Cao, J.Y. & Cai, X.Z. (2018) Leaf stage-associated resistance is correlated with phytohormones in a pathosystem-dependent manner. Journal of Integrative Plant Biology, 60, 703-722. Available from: https://doi.org/10.1111/jipb.12661
Yanai, O., Shani, E., Dolezal, K., Tarkowski, P., Sablowski, R., Sandberg, G. et al. (2005) Arabidopsis KNOXI proteins activate cytokinin biosynthesis. Current Biology, 15, 1566-1571. Available from: https://doi.org/10.1016/j.cub.2005.07.060
Yanai, O., Shani, E., Russ, D. & Ori, N. (2011) Gibberellin partly mediates LANCEOLATE activity in tomato. The Plant Journal, 68, 571-582. Available from: https://doi.org/10.1111/j.1365-313X.2011.04716.x
Yang, D.L., Li, Q., Deng, Y.W., Lou, Y.G., Wang, M.Y., Zhou, G.X. et al. (2008) Altered disease development in the eui mutants and Eui overexpressors indicates that gibberellins negatively regulate rice basal disease resistance. Molecular Plant, 1, 528-537. Available from: https://doi.org/10.1093/mp/ssn021
Ye, R., Wang, M., Du, H., Chhajed, S., Koh, J., Liu, K. et al. (2022) Glucose-driven TOR-FIE-PRC2 signalling controls plant development. Nature, 609, 986-993. Available from: https://doi.org/10.1038/s41586-022-05171-5
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. Available from: https://doi.org/10.1073/pnas.2015400117
Zeier, J. (2005) Age-dependent variations of local and systemic defence responses in Arabidopsis leaves towards an avirulent strain of Pseudomonas syringae. Physiological and Molecular Plant Pathology, 66, 30-39. Available from: https://doi.org/10.1016/j.pmpp.2005.03.007
Zhang, P. & Chen, K. (2009) Age-dependent variations of volatile emissions and inhibitory activity toward Botrytis cinerea and Fusarium oxysporum in tomato leaves treated with chitosan oligosaccharide. Journal of Plant Biology, 52, 332-339. Available from: https://doi.org/10.1007/s12374-009-9043-9
Zhang, Y., Zhang, Y., McFarlane, H.E., Obata, T., Richter, A.S., Lohse, M. et al. (2018) Inhibition of TOR represses nutrient consumption, which improves greening after extended periods of etiolation. Plant Physiology, 178, 101-117. Available from: https://doi.org/10.1104/pp.18.00684
Zhang, Z., Zhu, J.Y., Roh, J., Marchive, C., Kim, S.K., Meyer, C. et al. (2016) TOR signaling promotes accumulation of BZR1 to balance growth with carbon availability in Arabidopsis. Current Biology, 26, 1854-1860. Available from: https://doi.org/10.1016/j.cub.2016.05.005
Zürcher, E. & Müller, B. (2016) Cytokinin synthesis, signaling, and function-advances and new insights, International Review of Cell and Molecular Biology, 324. Elsevier Inc, pp. 1-38. https://doi.org/10.1016/bs.ircmb.2016.01.001
Zürcher, E., Tavor-Deslex, D., Lituiev, D., Enkerli, K., Tarr, P.T. & Müller, B. (2013) A robust and sensitive synthetic sensor to monitor the transcriptional output of the cytokinin signaling network in planta. Plant Physiology, 161, 1066-1075. Available from: https://doi.org/10.1104/pp.112.211763

Auteurs

Iftah Marash (I)

Department of Plant Pathology and Weed Research, Agricultural Research Organization, Volcani Institute, Bet Dagan, Israel.
School of Plant Science and Food Security, Tel-Aviv University, Tel-Aviv, Israel.

Rupali Gupta (R)

Department of Plant Pathology and Weed Research, Agricultural Research Organization, Volcani Institute, Bet Dagan, Israel.

Gautam Anand (G)

Department of Plant Pathology and Weed Research, Agricultural Research Organization, Volcani Institute, Bet Dagan, Israel.

Meirav Leibman-Markus (M)

Department of Plant Pathology and Weed Research, Agricultural Research Organization, Volcani Institute, Bet Dagan, Israel.

Naomi Lindner (N)

Department of Plant Pathology and Weed Research, Agricultural Research Organization, Volcani Institute, Bet Dagan, Israel.
Department of Plant Pathology and Microbiology, The Robert H. Smith Faculty of Agriculture, Food and Environment, The Hebrew University of Jerusalem, Rehovot, Israel.

Alon Israeli (A)

Institute of Plant Science and Genetics in Agriculture, The Robert H. Smith Faculty of Agriculture, Food and Environment, The Hebrew University of Jerusalem, Rehovot, Israel.

Dov Nir (D)

Institute of Plant Science and Genetics in Agriculture, The Robert H. Smith Faculty of Agriculture, Food and Environment, The Hebrew University of Jerusalem, Rehovot, Israel.

Adi Avni (A)

School of Plant Science and Food Security, Tel-Aviv University, Tel-Aviv, Israel.

Maya Bar (M)

Department of Plant Pathology and Weed Research, Agricultural Research Organization, Volcani Institute, Bet Dagan, Israel.

Classifications MeSH