Phloem exudate metabolic content reflects the response to water-deficit stress in pea plants (Pisum sativum L.)

. 2021 Jun ; 106 (5) : 1338-1355. [epub] 20210506

Jazyk angličtina Země Velká Británie, Anglie Médium print-electronic

Typ dokumentu časopisecké články, práce podpořená grantem

Perzistentní odkaz   https://www.medvik.cz/link/pmid33738886

Drought stress impacts the quality and yield of Pisum sativum. Here, we show how short periods of limited water availability during the vegetative stage of pea alters phloem sap content and how these changes are connected to strategies used by plants to cope with water deficit. We have investigated the metabolic content of phloem sap exudates and explored how this reflects P. sativum physiological and developmental responses to drought. Our data show that drought is accompanied by phloem-mediated redirection of the components that are necessary for cellular respiration and the proper maintenance of carbon/nitrogen balance during stress. The metabolic content of phloem sap reveals a shift from anabolic to catabolic processes as well as the developmental plasticity of P. sativum plants subjected to drought. Our study underlines the importance of phloem-mediated transport for plant adaptation to unfavourable environmental conditions. We also show that phloem exudate analysis can be used as a useful proxy to study stress responses in plants. We propose that the decrease in oleic acid content within phloem sap could be considered as a potential marker of early signalling events mediating drought response.

Zobrazit více v PubMed

Alfocea, F.P., Balibrea, M.E., Alarcón, J.J. & Bolarín, M.C. (2000) Composition of xylem and phloem exudates in relation to the salt‐tolerance of domestic and wild tomato species. Journal of Plant Physiology, 156, 367–374.

Alves‐Carvalho, S., Aubert, G., Carrere, S., Cruaud, C., Brochot, A.L., Jacquin, F. PubMed

Andersen, M.N. & Aremu, J.A. (1991) Drought sensitivity, root development and osmotic adjustment in field grown peas. Irrigation Science, 12, 45–51.

Andriankaja, M., Dhondt, S., De Bodt, S., Vanhaeren, H., Coppens, F., De Milde, L. PubMed

Aubry, E., Dinant, S., Vilaine, F., Bellini, C. & Le Hir, R. (2019) Lateral transport of organic and inorganic solutes. Plants, 8, 20. PubMed PMC

Avramova, V., AbdElgawad, H., Zhang, Z., Fotschki, B., Casadevall, R., Vergauwen, L. PubMed PMC

Aykas, D.P., Ball, C., Sia, A., Zhu, K., Shotts, M.‐L., Schmenk, A. PubMed PMC

Barbaglia, A.M. & Hoffmann‐Benning, S. (2016) Long‐distance lipid signaling and its role in plant development and stress response. In: Nakamura, Y. & Li‐Beisson, Y. (Eds) Lipids in Plant and Algae Development. Cham: Springer International Publishing, pp. 339–361. PubMed

Braidwood, L., Breuer, C. & Sugimoto, K. (2014) My body is a cage: mechanisms and modulation of plant cell growth. New Phytologist, 201, 388–402. PubMed

Buhtz, A., Springer, F., Chappell, L., Baulcombe, D.C. & Kehr, J. (2008) Identification and characterization of small RNAs from the phloem of PubMed

Cal, A.J., Sanciangco, M., Rebolledo, M.C., Luquet, D., Torres, R.O., McNally, K.L. PubMed PMC

Canarini, A., Merchant, A. & Dijkstra, F.A. (2016) Drought effects on

Clauw, P., Coppens, F., Korte, A., Herman, D., Slabbinck, B., Dhondt, S. PubMed PMC

Coller, B.S. (2015) Blood at 70: its roots in the history of hematology and its birth. Blood, 126, 2548–2560. PubMed PMC

de Reuille, P.B. & Ragni, L. (2017) Vascular morphodynamics during secondary growth. In: de Lucas, M. & Etchhells, J. (Eds) Xylem, Vol 1544. Methods in Molecular Biology. New York, NY: Humana Press, pp. 103–125. 10.1007/978-1-4939-6722-3_10 PubMed DOI

Dinant, S., Bonnemain, J.‐L., Girousse, C. & Kehr, J. (2010) Phloem sap intricacy and interplay with aphid feeding. Comptes Rendus Biologies, 333, 504–515. PubMed

Dinant, S. & Suárez‐López, P. (2012) Multitude of Long‐Distance Signal Molecules Acting Via Phloem. 14, 89–121.

Gamboa‐Tuz, S.D., Pereira‐Santana, A., Zamora‐Briseño, J.A., Castano, E., Espadas‐Gil, F., Ayala‐Sumuano, J.T. PubMed PMC

Gessler, A., Rennenberg, H. & Keitel, C. (2004) Stable isotope composition of organic compounds transported in the phloem of European beech – evaluation of different methods of phloem sap collection and assessment of gradients in carbon isotope composition during leaf‐to‐stem transport. Plant Biology, 6, 721–729. PubMed

Giavalisco, P., Kapitza, K., Kolasa, A., Buhtz, A. & Kehr, J. (2006) Towards the proteome of PubMed

Gowan, E., Lewis, B.A. & Turgeon, R. (1995) Phloem transport of antirrhinoside, an iridoid glycoside, in PubMed

Hildebrandt, T.M., Nunes Nesi, A., Araújo, W.L. & Braun, H.‐P. (2015) Amino acid catabolism in plants. Molecular Plant, 8, 1563–1579. PubMed

Kehr, J. & Kragler, F. (2018) Long distance RNA movement. New Phytologist, 218, 29–40. PubMed

Keitel, C., Matzarakis, A., Rennenberg, H. & Gessler, A. (2006) Carbon isotopic composition and oxygen isotopic enrichment in phloem and total leaf organic matter of European beech ( PubMed

Kind, T., Wohlgemuth, G., Lee, D.Y., Lu, Y., Palazoglu, M., Shahbaz, S. PubMed PMC

Kircher, S. & Schopfer, P. (2012). Photosynthetic sucrose acts as cotyledon‐derived long‐distance signal to control root growth during early seedling development in PubMed PMC

Kirkham, M.B. (2014) Field Capacity, Wilting Point, Available Water, and the Nonlimiting Water Range. 153–170.

Klimek‐Kopyra, A., Zając, T., Skowera, B. & Styrc, N. (2017) The effect of water shortage on pea (

Kollist, H., Zandalinas, S.I., Sengupta, S., Nuhkat, M., Kangasjärvi, J. & Mittler, R. (2019) Rapid responses to abiotic stress: priming the landscape for the signal transduction network. Trends in Plant Science, 24, 25–37. PubMed

Kuwabara, A., Backhaus, A., Malinowski, R., Bauch, M., Hunt, L., Nagata, T. PubMed PMC

Lalonde, S., Tegeder, M., Throne‐Holst, M., Frommer, W.B. & Patrick, J.W. (2003) Phloem loading and unloading of sugars and amino acids. Plant, Cell & Environment, 26, 37–56.

Lemoine, R., Camera, S.L., Atanassova, R., Dédaldéchamp, F., Allario, T., Pourtau, N. PubMed PMC

López‐Salmerón, V., Cho, H., Tonn, N. & Greb, T. (2019) The phloem as a mediator of plant growth plasticity. Current Biology, 29, R173–R181. PubMed

Majumdar, R., Barchi, B., Turlapati, S.A., Gagne, M., Minocha, R., Long, S. PubMed PMC

Malter, D. & Wolf, S. (2011) Melon phloem‐sap proteome: developmental control and response to viral infection. Protoplasma, 248, 217–224. PubMed

Mandal, M.K., Chandra‐Shekara, A.C., Jeong, R.‐D., Yu, K., Zhu, S., Chanda, B. PubMed PMC

Marchetti, C.F., Ugena, L., Humplík, J.F., Polák, M., Ćavar, Z.S., Podlešáková, K. PubMed DOI PMC

Merchant, A. (2012) Developing phloem d 13 C and sugar composition as indicators of water deficit in

Michaeli, S. & Fromm, H. (2015) Closing the loop on the GABA shunt in plants: are GABA metabolism and signaling entwined? Frontiers in plant science, 6, 419. PubMed PMC

Mundim, F.M. & Pringle, E.G. (2018) Whole‐plant metabolic allocation under water stress. Frontiers in plant science, 9, 852. PubMed PMC

Noonan, M.J., Tinnesand, H.V. & Buesching, C.D. (2018) Normalizing gas‐chromatography–mass spectrometry data: method choice can alter biological inference. BioEssays, 40, 1700210. PubMed

Ouaked, F., Rozhon, W., Lecourieux, D. & Hirt, H. (2003) A MAPK pathway mediates ethylene signaling in plants. The EMBO Journal, 22, 1282–1288. PubMed PMC

Pahlow, S., Ostendorp, A., Krüßel, L. & Kehr, J. (2018) Phloem sap sampling from PubMed PMC

Pate, J.S. & Atkins, C.A. (1983) Xylem and phloem transport and the functional economy of carbon and nitrogen of a legume leaf. Plant Physiology, 71, 835–840. PubMed PMC

Pfaffl, M.W., Horgan, G.W. & Dempfle, L. (2002) Relative expression software tool (REST PubMed PMC

Pirasteh‐Anosheh, H., Saed‐Moucheshi, A., Pakniyat, H. & Pessarakli, M. (2016) Stomatal responses to drought stress. In: Ahmad, P. (Ed.) Water Stress and Crop Plants: A Sustainable Approach. John Wiley & Sons, Ltd., pp. 24–40.

Podlešáková, K., Ugena, L., Spíchal, L., Doležal, K. & De Diego, N. (2019) Phytohormones and polyamines regulate plant stress responses by altering GABA pathway. New Biotechnology, 48, 53–65. PubMed

Regnault, T., Davière, J.‐M., Wild, M., Sakvarelidze‐Achard, L., Heintz, D., Carrera Bergua, E. PubMed

Rocha, M., Licausi, F., Araújo, W.L., Nunes‐Nesi, A., Sodek, L., Fernie, A.R. PubMed PMC

Sack, L. & Scoffoni, C. (2013) Leaf venation: structure, function, development, evolution, ecology and applications in the past, present and future. New Phytologist, 198, 983–1000. PubMed

Sankar, M., Nieminen, K., Ragni, L., Xenarios, I. & Hardtke, C.S. (2014) Automated quantitative histology reveals vascular morphodynamics during Arabidopsis hypocotyl secondary growth. eLife, 3, e01567. PubMed PMC

Savage, J.A., Zwieniecki, M.A. & Holbrook, N.M. (2013) Phloem transport velocity varies over time and among vascular bundles during early cucumber seedling development. Plant Physiology, 163, 1409–1418. PubMed PMC

Schneider, C.A., Rasband, W.S. & Eliceiri, K.W. (2012) NIH Image to ImageJ: 25 years of image analysis. Nature Methods, 9, 671. PubMed PMC

Sevanto, S. (2014) Phloem transport and drought. Journal of Experimental Botany, 65, 1751–1759. PubMed

Sevanto, S. (2018) Drought impacts on phloem transport. Current Opinion in Plant Biology, 43, 76–81. PubMed

Sevanto, S., McDowell, N.G., Dickman, L.T., Pangle, R. & Pockman, W.T. (2014) How do trees die? A test of the hydraulic failure and carbon starvation hypotheses. Plant, Cell & Environment, 37, 153–161. PubMed PMC

Sharma, S., Villamor, J.G. & Verslues, P.E. (2011) Essential role of tissue‐specific proline synthesis and catabolism in growth and redox balance at low water potential. Plant Physiology, 157, 292–304. PubMed PMC

Siqueira, J.A., Hardoim, P., Ferreira, P.C.G., Nunes‐Nesi, A. & Hemerly, A.S. (2018) Unraveling interfaces between energy metabolism and cell cycle in plants. Trends in Plant Science, 23, 731–747. PubMed

Sirault, X.R.R., James, R.A. & Furbank, R.T. (2009) A new screening method for osmotic component of salinity tolerance in cereals using infrared thermography. Functional Plant Biology, 36, 970–977. PubMed

Stroock, A.D., Pagay, V.V., Zwieniecki, M.A. & Holbrook, N.M. (2014) The physicochemical hydrodynamics of vascular plants. Annual Review of Fluid Mechanics, 46, 615–642.

Takahashi, F. & Shinozaki, K. (2019) Long‐distance signaling in plant stress response. Current Opinion in Plant Biology, 47, 106–111. PubMed

Tetyuk, O., Benning, U.F. & Hoffmann‐Benning, S. (2013) Collection and analysis of Arabidopsis phloem exudates using the EDTA‐facilitated method. Journal of Visualized Experiments, 80, e51111. PubMed PMC

Tilsner, J., Kassner, N., Struck, C. & Lohaus, G. (2005) Amino acid contents and transport in oilseed rape ( PubMed

Toyota, M., Spencer, D., Sawai‐Toyota, S., Jiaqi, W., Zhang, T., Koo, A.J. PubMed

van Bel, A.J.E. & Hess, P.H. (2008) Hexoses as phloem transport sugars: the end of a dogma? Journal of Experimental Botany, 59, 261–272. PubMed

Wunderling, A., Ben Targem, M., Barbier de Reuille, P. & Ragni, L. (2016) Novel tools for quantifying secondary growth. Journal of Experimental Botany, 68, 89–95. PubMed

Yamaguchi‐Shinozaki, K. & Shinozaki, K. (1993) Characterization of the expression of a desiccation‐responsive rd29 gene of Arabidopsis thaliana and analysis of its promoter in transgenic plants. Molecular & General Genetics, 236–236, 331–340. PubMed

Yamamoto, R., Inouhe, M. & Masuda, Y. (1988) Galactose inhibition of auxin‐induced growth of mono‐ and dicotyledonous plants. Plant Physiology, 86, 1223–1227. PubMed PMC

Yang, X., Neta, P. & Stein, S.E. (2017) Extending a tandem mass spectral library to include MS(2) spectra of fragment ions produced in‐source and MS(n) spectra. Journal of the American Society for Mass Spectrometry, 28, 2280–2287. PubMed

Zhong, W., Hartung, W., Komor, E. & Schobert, C. (1996) Phloem transport of abscisic acid in

Najít záznam

Citační ukazatele

Nahrávání dat ...

Možnosti archivace

Nahrávání dat ...