Exogenous strigolactones impact metabolic profiles and phosphate starvation signalling in roots.
2′-epi-GR24
Pi starvation
metabolism
molecular markers
plant responses
signalling
strigolactones
Journal
Plant, cell & environment
ISSN: 1365-3040
Titre abrégé: Plant Cell Environ
Pays: United States
ID NLM: 9309004
Informations de publication
Date de publication:
07 2020
07 2020
Historique:
received:
18
01
2020
revised:
09
03
2020
accepted:
11
03
2020
pubmed:
31
3
2020
medline:
11
2
2021
entrez:
31
3
2020
Statut:
ppublish
Résumé
Strigolactones (SLs) are important ex-planta signalling molecules in the rhizosphere, promoting the association with beneficial microorganisms, but also affecting plant interactions with harmful organisms. They are also plant hormones in-planta, acting as modulators of plant responses under nutrient-deficient conditions, mainly phosphate (Pi) starvation. In the present work, we investigate the potential role of SLs as regulators of early Pi starvation signalling in plants. A short-term pulse of the synthetic SL analogue 2'-epi-GR24 promoted SL accumulation and the expression of Pi starvation markers in tomato and wheat under Pi deprivation. 2'-epi-GR24 application also increased SL production and the expression of Pi starvation markers under normal Pi conditions, being its effect dependent on the endogenous SL levels. Remarkably, 2'-epi-GR24 also impacted the root metabolic profile under these conditions, promoting the levels of metabolites associated to plant responses to Pi limitation, thus partially mimicking the pattern observed under Pi deprivation. The results suggest an endogenous role for SLs as Pi starvation signals. In agreement with this idea, SL-deficient plants were less sensitive to this stress. Based on the results, we propose that SLs may act as early modulators of plant responses to P starvation.
Substances chimiques
GR24 strigolactone
0
Heterocyclic Compounds, 3-Ring
0
Lactones
0
Phosphates
0
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
1655-1668Informations de copyright
© 2020 John Wiley & Sons Ltd.
Références
Al-Babili, S., & Bouwmeester, H. J. (2015). Strigolactones, a novel carotenoid-derived plant hormone. In Annual review of plant biology (Vol. 66, pp. 161-186). Palo Alto, CA: Annual Reviews.
Andreo-Jiménez, B., Ruyter-Spira, C., Bouwmeester, H., & López-Ráez, J. A. (2015). Ecological relevance of strigolactones in nutrient uptake and other abiotic stresses, and in plant-microbe interactions below-ground. Plant and Soil, 394, 1-19. https://doi.org/10.1007/s11104-015-2544-z
Bustos, R., Castrillo, G., Linhares, F., Puga, M. I., Rubio, V., Pérez-Pérez, J., … Paz-Ares, J. (2010). A central regulatory system largely controls transcriptional activation and repression responses to phosphate starvation in Arabidopsis. PLoS Genetics, 6, e1001102. https://doi.org/10.1371/journal.pgen.1001102
Campos, P., Borie, F., Cornejo, P., López-Ráez, J. A., López-García, A., & Seguel, A. (2018). Phosphorus acquisition efficiency related to root traits: Is mycorrhizal symbiosis a key factor to wheat and barley cropping? Frontiers in Plant Science, 9, 1-21. https://doi.org/10.3389/fpls.2018.00752
de Souza Campos, P. M., Cornejo, P., Rial, C., Borie, F., Varela, R. M., Seguel, A., & Lopez-Raez, J. A. (2019). Phosphate acquisition efficiency in wheat is related to root: Shoot ratio, strigolactone levels, and Pho2 regulation. Journal of Experimental Botany, 70, 5631-5642. https://doi.org/10.1093/jxb/erz349
Chiou, T. J., & Lin, S. I. (2011). Signaling network in sensing phosphate availability in plants. In Annual review of plant biology (Vol. 62, pp. 185-206). Palo Alto, CA: Annual Reviews.
Chong, J., & Xia, J. (2018). MetaboAnalystR: An R package for flexible and reproducible analysis of metabolomics data. Bioinformatics (Oxford, England), 34, 4313-4314. https://doi.org/10.1093/bioinformatics/bty528
De Cuyper, C., Fromentin, J., Yocgo, R. E., De Keyser, A., Guillotin, B., Kunert, K., … Goormachtig, S. (2015). From lateral root density to nodule number, the strigolactone analogue GR24 shapes the root architecture of Medicago truncatula. Journal of Experimental Botany, 66, 137-146. https://doi.org/10.1093/jxb/eru404
Franco-Zorrilla, J. M., Valli, A., Todesco, M., Mateos, I., Puga, M. I., Rubio-Somoza, I., … Paz-Ares, J. (2007). Target mimicry provides a new mechanism for regulation of microRNA activity. Nature Genetics, 39, 1033-1037. https://doi.org/10.1038/ng2079
Gamir, J., Pastor, V., Cerezo, M., & Flors, V. (2012). Identification of indole-3-carboxylic acid as mediator of priming against Plectosphaerella cucumerina. Plant Physiology and Biochemistry, 61, 169-179. https://doi.org/10.1016/j.plaphy.2012.10.004
Gómez-Roldán, V., Fermas, S., Brewer, P. B., Puech-Pagés, V., Dun, E. A., Pillot, J. P., … Rochange, S. F. (2008). Strigolactone inhibition of shoot branching. Nature, 455, 189-194. https://doi.org/10.1038/nature07271
Grün, A., Buchner, P., Broadley, M. R., & Hawkesford, M. J. (2018). Identification and expression profiling of Pht1 phosphate transporters in wheat in controlled environments and in the field. Plant Biology, 20(2), 374-389. https://doi.org/10.1111/plb.12668
Ham, B. K., Chen, J., Yan, Y., & Lucas, W. J. (2018). Insights into plant phosphate sensing and signaling. Current Opinion in Biotechnology, 49, 1-9. https://doi.org/10.1016/j.copbio.2017.07.005
Hewitt, E. J. (1966). Sand and water culture methods used in the study of plant nutrition. Paper presented at the Technical communication no. 22. Commonwealth Agriculture Bureau, London, UK.
Huang, T. K., Han, C. L., Lin, S. I., Chen, Y. J., Tsai, Y. C., Chen, Y. R., … Chiou, T. J. (2013). Identification of downstream components of ubiquitin-conjugating enzyme PHOSPHATE2 by quantitative membrane proteomics in Arabidopsis roots. Plant Cell, 25, 4044-4060. https://doi.org/10.1105/tpc.113.115998
Ito, S., Nozoye, T., Sasaki, E., Imai, M., Shiwa, Y., Shibata-Hatta, M., … Asami, T. (2015). Strigolactone regulates anthocyanin accumulation, acid phosphatases production and plant growth under low phosphate condition in Arabidopsis. PLoS One, 10, e0119724. https://doi.org/10.1371/journal.pone.0119724
Jung, H. W., Tschaplinski, T. J., Wang, L., Glazebrook, J., & Greenberg, J. T. (2009). Priming in systemic plant immunity. Science, 324, 89-91. https://doi.org/10.1126/science.1170025
Kaever, A., Landesfeind, M., Feussner, K., Mosblech, A., Heilmann, I., Morgenstern, B., … Meinicke, P. (2015). MarVis-pathway: Integrative and exploratory pathway analysis of non-targeted metabolomics data. Metabolomics, 11, 764-777. https://doi.org/10.1007/s11306-014-0734-y
Kapulnik, Y., Delaux, P. M., Resnick, N., Mayzlish-Gati, E., Wininger, S., Bhattacharya, C., … Koltai, H. (2011). Strigolactones affect lateral root formation and root-hair elongation in Arabidopsis. Planta, 233, 209-216.
Khan, G. A., Vogiatzaki, E., Glauser, G., & Poirier, Y. (2016). Phosphate deficiency induces the jasmonate pathway and enhances resistance to insect herbivory. Plant Physiology, 171, 632-644. https://doi.org/10.1104/pp.16.00278
Kohlen, W., Charnikhova, T., Lammers, M., Pollina, T., Toth, P., Haider, I., … López-Ráez, J. A. (2012). The tomato CAROTENOID CLEAVAGE DIOXYGENASE8 (SlCCD8) regulates rhizosphere signaling, plant architecture and affects reproductive development through strigolactone biosynthesis. New Phytologist, 196, 535-547. https://doi.org/10.1111/j.1469-8137.2012.04265.x
Lambers, H., Martinoia, E., & Renton, M. (2015). Plant adaptations to severely phosphorus-impoverished soils. Current Opinion in Plant Biology, 25, 23-31. https://doi.org/10.1016/j.pbi.2015.04.002
Lan, P., Li, W., & Schmidt, W. (2015). ‘Omics’ approaches towards understanding plant phosphorus acquisition and use. In W. C. Plaxton & H. Lambers (Eds.), Phosphorus metabolism in plants (Vol. 48, pp. 65-98). Nueva Jersey (USA): Annual Plant Reviews (John Wiley & Sons).
Lin, S. I., Chiang, S. F., Lin, W. Y., Chen, J. W., Tseng, C. Y., Wu, P. C., & Chiou, T. J. (2008). Regulatory network of microRNA399 and PHO2 by systemic signaling. Plant Physiology, 147, 732-746. https://doi.org/10.1104/pp.108.116269
Liu, C. M., Muchhal, U. S., & Raghothama, K. G. (1997). Differential expression of TPS11, a phosphate starvation-induced gene in tomato. Plant Molecular Biology, 33, 867-874. https://doi.org/10.1023/A:1005729309569
Liu, T. Y., Huang, T. K., Tseng, C. Y., Lai, Y. S., Lin, S. I., Lin, W. Y., … Chioua, T. J. (2012). PHO2-dependent degradation of PHO1 modulates phosphate homeostasis in Arabidopsis. Plant Cell, 24, 2168-2183. https://doi.org/10.1105/tpc.112.096636
Livak, K. J., & Schmittgen, T. D. (2001). Analysis of relative gene expression data using real-time quantitative PCR and the 2_DDCt method. Methods, 25, 402-408. https://doi.org/10.1006/meth.2001.1262
López-Ráez, J. A., Charnikhova, T., Gómez-Roldán, V., Matusova, R., Kohlen, W., De Vos, R., … Bouwmeester, H. (2008). Tomato strigolactones are derived from carotenoids and their biosynthesis is promoted by phosphate starvation. New Phytologist, 178, 863-874. https://doi.org/10.1111/j.1469-8137.2008.02406.x
López-Ráez, J. A., Charnikhova, T., Mulder, P., Kohlen, W., Bino, R., Levin, I., & Bouwmeester, H. (2008). Susceptibility of the tomato mutant high pigment-2dg (hp-2dg) to Orobanche spp infection. Journal of Agricultural and Food Chemistry, 56, 6326-6332.
López-Ráez, J. A., Shirasu, K., & Foo, E. (2017). Strigolactones in plant interactions with beneficial and detrimental organisms: The yin and yang. Trends in Plant Science, 22, 527-537. https://doi.org/10.1016/j.tplants.2017.03.011
Lynch, J. P. (2011). Root phenes for enhanced soil exploration and phosphorus acquisition: Tools for future crops. Plant Physiology, 156, 1041-1049. https://doi.org/10.1104/pp.111.175414
Medici, A., Szponarski, W., Dangeville, P., Safi, A., Dissanayake, I. M., Saenchai, C., … Krouk, G. (2019). Identification of molecular integrators shows that nitrogen actively controls the phosphate starvation response in plants. Plant Cell, 31(5), 1171-1184. https://doi.org/10.1105/tpc.18.00656
Mora-Macías, J., Ojeda-Rivera, J. O., Gutiérrez-Alanís, D., Yong-Villalobos, L., Oropeza-Aburto, A., Raya-González, J., … Herrera-Estrell, L. (2017). Malate-dependent Fe accumulation is a critical checkpoint in the root developmental response to low phosphate. Proceedings of the National Academy of Sciences of the United States of America, 114, E3563-E3572. https://doi.org/10.1073/pnas.1701952114
Nagy, F., Karandashov, V., Chague, W., Kalinkevich, K., Tamasloukht, M., Xu, G. H., … Bucher, M. (2005). The characterization of novel mycorrhiza-specific phosphate transporters from Lycopersicon esculentum and Solanum tuberosum uncovers functional redundancy in symbiotic phosphate transport in solanaceous species. Plant Journal, 42, 236-250. https://doi.org/10.1111/j.1365-313X.2005.02364.x
Pant, B. D., Buhtz, A., Kehr, J., & Scheible, W. R. (2008). MicroRNA399 is a long-distance signal for the regulation of plant phosphate homeostasis. Plant Journal, 53, 731-738. https://doi.org/10.1111/j.1365-313X.2007.03363.x
Pant, B. D., Pant, P., Erban, A., Huhman, D., Kopka, J., & Scheible, W. R. (2015). Identification of primary and secondary metabolites with phosphorus status-dependent abundance in Arabidopsis, and of the transcription factor PHR1 as a major regulator of metabolic changes during phosphorus limitation. Plant Cell and Environment, 38, 172-187. https://doi.org/10.1111/pce.12378
Pérez-Torres, C. A., López-Bucio, J., Cruz-Ramírez, A., Ibarra-Laclette, E., Dharmasiri, S., Estelle, M., & Herrera-Estrella, L. (2008). Phosphate availability alters lateral root development in Arabidopsis by modulating auxin sensitivity via a mechanism involving the TIR1 auxin receptor. Plant Cell, 20, 3258-3272. https://doi.org/10.1105/tpc.108.058719
Prerostova, S., Kramna, B., Dobrev, P. I., Gaudinova, A., Marsik, P., Fiala, R., … Vankova, R. (2018). Organ-specific hormonal cross-talk in phosphate deficiency. Environmental and Experimental Botany, 153, 198-208. https://doi.org/10.1016/j.envexpbot.2018.05.020
Puga, M. I., Rojas-Triana, M., de Lorenzo, L., Leyva, A., Rubio, V., & Paz-Ares, J. (2017). Novel signals in the regulation of Pi starvation responses in plants: Facts and promises. Current Opinion in Plant Biology, 39, 40-49. https://doi.org/10.1016/j.pbi.2017.05.007
Raghothama, K. G. (2000). Phosphate transport and signaling. Current Opinion in Plant Biology, 3(3), 182-187. https://doi.org/10.1016/s1369-5266(00)80063-1
Rial, C., Varela, R. M., Molinillo, J. M. G., López Ráez, J. A., & Macías, F. A. (2009). A new UHPLC-MS/MS method for the direct determination of strigolactones in root exudates and extracts. Phytochemical Analysis, 30, 110-116. https://doi.org/10.1002/pca.2796
Rivero, J., Álvarez, D., Flors, V., Azcón-Aguilar, C., & Pozo, M. J. (2018). Root metabolic plasticity underlies functional diversity in mycorrhiza-enhanced stress tolerance in tomato. New Phytologist, 220, 1322-1336. https://doi.org/10.1111/nph.15295
Rubio, V., Linhares, F., Solano, R., Martín, A. C., Iglesias, J., Leyva, A., & Paz-Ares, J. (2001). A conserved MYB transcription factor involved in phosphate starvation signaling both in vascular plants and in unicellular algae. Genes & Development, 15, 2122-2133. https://doi.org/10.1101/gad.204401
Ruyter-Spira, C., Kohlen, W., Charnikhova, T., van Zeijl, A., van Bezouwen, L., de Ruijter, N., … Bouwmeester, H. (2011). Physiological effects of the synthetic strigolactone analog GR24 on root system architecture in Arabidopsis: Another belowground role for strigolactones? Plant Physiology, 155, 721-734. https://doi.org/10.1104/pp.110.166645
Scaffidi, A., Waters, M. T., Sun, Y. K., Skelton, B. W., Dixon, K. W., Ghisalberti, E. L., … Smith, S. M. (2014). Strigolactone hormones and their stereoisomers signal through two related receptor proteins to induce different physiological responses in Arabidopsis. Plant Physiology, 165, 1221-1232. https://doi.org/10.1104/pp.114.240036
Scheible, W. R., & Rojas-Triana, M. (2015). Sensing, signalling, and control of phosphate starvation in plants: Molecular players and applications. In W. C. Plaxton & H. Lambers (Eds.), Phosphorus metabolism in plants (Vol. 48, pp. 25-64). Nueva Jersey (USA): Annual Plant Reviews (John Wiley & Sons).
Secco, D., Wang, C., Arpat, B. A., Wang, Z., Poirier, Y., Tyerman, S. D., … Whelan, J. (2012). The emerging importance of the SPX domain-containing proteins in phosphate homeostasis. New Phytologist, 193, 842-851. https://doi.org/10.1111/j.1469-8137.2011.04002
Song, L., Yu, H., Dong, J., Che, X., Jiao, Y., & Liu, D. (2016). The molecular mechanism of ethylene-mediated root hair development induced by phosphate starvation. PLoS Genetics, 12, e1006194. https://doi.org/10.1371/journal.pgen.1006194
Stes, E., Depuydt, S., De Keyser, A., Matthys, C., Audenaert, K., Yoneyama, K., … Vereecke, D. (2015). Strigolactones as an auxiliary hormonal defence mechanism against leafy gall syndrome in Arabidopsis thaliana. Journal of Experimental Botany, 66, 5123-5134. https://doi.org/10.1093/jxb/erv309
Torres-Vera, R., García, J. M., Pozo, M. J., & López-Ráez, J. A. (2014). Do strigolactones contribute to plant defence? Molecular Plant Pathology, 15, 211-216. https://doi.org/10.1111/mpp.12074
Umehara, M., Hanada, A., Yoshida, S., Akiyama, K., Arite, T., Takeda-Kamiya, N., … Yamaguchi, S. (2008). Inhibition of shoot branching by new terpenoid plant hormones. Nature, 455, 195-200. https://doi.org/10.1038/nature07272
Wang, G. Y., Shi, J. L., Ng, G., Battle, S. L., Zhang, C., & Lu, H. (2011). Circadian clock-regulated phosphate transporter PHT4;1 plays an important role in Arabidopsis defense. Molecular Plant, 4, 516-526. https://doi.org/10.1093/mp/ssr016
Waters, M. T., Gutjahr, C., Bennett, T., & Nelson, D. C. (2017). Strigolactone signaling and evolution. In Annual review of plant biology (Vol. 68, pp. 291-322). Palo Alto, CA: Annual Reviews.
Yoneyama, K., Xie, X., Kim, H. I., Kisugi, T., Nomura, T., Sekimoto, H., … Yoneyama, K. (2012). How do nitrogen and phosphorus deficiencies affect strigolactone production and exudation? Planta, 235, 1197-1207. https://doi.org/10.1007/s00425-011-1568-8
Zhou, J., Jiao, F., Wu, Z., Li, Y., Wang, X., He, X., … Wu, P. (2008). OsPHR2 is involved in phosphate-starvation signaling and excessive phosphate accumulation in shoots of plants. Plant Physiology, 146, 1673-1686. https://doi.org/10.1104/pp.107.111443
Ziegler, J., Schmidt, S., Chutia, R., Müller, J., Böttcher, C., Strehmel, N., … Abel, S. (2016). Non-targeted profiling of semi-polar metabolites in Arabidopsis root exudates uncovers a role for coumarin secretion and lignification during the local response to phosphate limitation. Journal of Experimental Botany, 67, 1421-1432. https://doi.org/10.1093/jxb/erv539