Distinct physiological mechanisms underpin growth and rehydration of Hymenaea courbaril and Hymenaea stigonocarpa upon short-term exposure to drought stress

doi:10.1007/s11676-022-01558-2

摘要/Abstract

Abstract:

Plants hold biochemical and physiological mechanisms to withstand drought conditions. Generally, depending on water deficit interval, plant rehydration relies on how it can retain growth or a positive water balance—or rarely both. In this study, two species of Hymenaea, one from the Amazon and the other from the Brazilian Cerrado, were investigated for their physiological mechanism associated with growth rehydration upon short-term exposure to drought stress. Our findings demonstrate that Hymenaea courbaril tends to invest in nitrogen to the detriment of carbon compounds, − as it is limited by lower net photosynthesis − and adjust root growth to attenuate drought stress responses. In contrast, Hymenaea stigonocarpa takes advantage of higher water potential and a basal rate of lower net photosynthesis to support aboveground growth under such conditions. Hence, it is postulated that there are distinct ways of controlling water status and growth between H. courbaril and H. stigonocarpa, which are determined either by the ability of the species to keep net photosynthesis at low levels of water content or by favoring the accumulation of nitrogen compounds. Both mechanisms were effective with regards to water use efficiency and thus it is reasonable to suggest that strategies are not exclusive and may work under adverse conditions, as observed in Amazon and Brazilian Cerrado biomes.Query

Key words: Hymenaea courbaril, Hymenaea stigonocarpa, Growth, Photosynthesis, Water deficit

Luana M. Luz, Ediane C. Alves, Nariane Q. Vilhena, Tamires B. Oliveira, Zara G. B. Silva, Joze M. N. Freitas, Cândido F. O. Neto, Roberto C. L. Costa, Lucas C. Costa. [J]. 林业研究(英文版), 2023, 34(1): 113-123.

Luana M. Luz, Ediane C. Alves, Nariane Q. Vilhena, Tamires B. Oliveira, Zara G. B. Silva, Joze M. N. Freitas, Cândido F. O. Neto, Roberto C. L. Costa, Lucas C. Costa. Distinct physiological mechanisms underpin growth and rehydration of Hymenaea courbaril and Hymenaea stigonocarpa upon short-term exposure to drought stress[J]. JOURNAL OF FORESTRY RESEARCH, 2023, 34(1): 113-123.

参考文献 72

1	Alves WF, Roig H, Kalin L, Prado LF, Valdir FS, Steinke A (2022) Analyzing trends in rainfall and their impacts in water management in a Cerrado region in Brazil. Research Square - Preprint. Available on https://doi.org/10.21203/rs.3.rs-830788/v1 [Accessed on June 21, 2022]
2	Al-Yasi H, Attia H, Alamer K, Hassan F, Ali E, Elshazly S, Siddique KH, Hessini K, Esmat F. Impact of drought on growth, photosynthesis, osmotic adjustment, and cell wall elasticity in Damask rose. Plant Physiol Biochem, 2020, 150: 133-139, DOI
3	Anjum SA, Ashraf U, Tanveer M, Khan I, Hussain S, Shahzad B, Zohaib A, Abbas F, Saleem MF, Ali I, Wang LC. Drought induced changes in growth, osmolyte accumulation and antioxidant metabolism of three maize hybrids. Front Plant Sci, 2017, 8: 69, DOI
4	Blackman CJ, Brodribb TJ. Two measures of leaf capacitance: insights into the water transport pathway and hydraulic conductance in leaves. Funct Plant Biol, 2011, 38: 118-126, DOI
5	Blum A. Osmotic adjustment is a prime drought stress adaptive engine in supportof plant production. Plant Cell Environ, 2017, 40: 4-10, DOI
6	Brito AEA, Palheta JG, Andresa CAS. Growth and ecophysiological aspects in young plants of Hymenaea courbaril L submitted to water stress and flooding. Int J Curr Res, 2016, 8(7): 34647-34654
7	Brunner I, Herzog C, Dawes MA, Arend M, Sperisen C. How tree roots respond to drought. Front Plant Sci, 2015, 6: 547, DOI
8	Caballero CB, Ruhoff A, Biggs T. Land use and land cover changes and their impacts on surface-atmosphere interactions in Brazil: A systematic review. Sci Total Environ, 2022, 808: 134-152, DOI
9	Carvalho PER. Galvao APM. Produção de mudas de espécies nativas por sementes e a implantação de povoamentos. Reflorestamento de propriedades rurais para fins produtivos e ambientais: um guia para ações municipais e regionais, 2000 Brasilia Colombo 151-174
10	Carvalho PER. Jatobá-do-serrado. Taxonomia e nomenclatura. Circular técnico 133, 2007 Brasília Embrapa Florestas 8
11	Catuchi TA, Vítolo HF, Bertolli SC, Souza GM. Tolerance to water deficiency between two soybean cultivars: transgenic versus conventional. Ciênc Rural, 2011, 31: 373-378, DOI
12	Chakhchar A, Lamaoui M, Wahbi S, Ferradous A, El Mousadik A, Ibnsouda Koraichi S, Filali-Maltouf A, El Modafar C. Leaf water status, osmoregulation and secondary metabolism as a model for depicting drought tolerance in Argania spinosa. Acta Physiol Plant, 2015, 37: 1-16, DOI
13	Chakhchar A, Lamaoui M, Aissam S, Ferradous A, Wahbi S, El Mousadik A, Ibnsouda Koraichi S, Filali-Maltouf A, El Modafar C. Differential physiological and antioxidative responses to drought stress and recovery among four contrasting Argania spinosa ecotypes. J Plant Interact, 2016, 11: 30-40, DOI
14	Chakhchar A, Haworth M, El Modafar C, Lauteri M, Mattioni C, Wahbi S, Centritto M. An assessment of genetic diversity and drought tolerance in argan tree (Argania spinosa) populations: potential for the development of improved drought tolerance. Front Plant Sci, 2017, 8: 276, DOI
15	Chakhchar A, Lamaoui M, Aissam S, Ferradous A, Wahbi S, El Mousadik A, Ibnsouda-Koraichi S, Filali-Maltouf A, El Modafar C. Physiological and biochemical mechanisms of drought stress tolerance in the argan tree. Plant Metabolites and Regulation Under Environmental Stress, 2018 Elsevier 311-322, DOI
16	Cosgrove DJ. Plant cell wall extensibility: connecting plant cell growth with cell wall structure, mechanics, and the action of wall-modifying enzymes. J Exp Bot, 2016, 67: 463-476, DOI
17	Cosgrove DJ. Catalysts of plant cell wall loosening. F1000Res, 2016, 5: 119, DOI
18	De Souza LC, Luz LM, Silva Martins JT, Oliveira Neto CF, Palheta JG, Oliveira TB, Alves CE, Almeida RF, Oliveira RLL, Costa RCL, Vilhena NQ. Osmoregulators in Hymenaea courbaril and Hymenaea stigonocarpa under water stress and rehydration. J for Res, 2018, 29(6): 1475-1479, DOI
19	Dubois M, Gilles KA, Hamilton JK, Rebers PA, Smith F. Colorimetric method for determination of sugars and related substances. Anal Chem, 1956, 28(3): 350-356, DOI
20	Erice GS, Louahlia JJ, Irigoyen M, Sanchez-Diaz JC. Biomass partitioning, morphology and water status of four alfalfa genotypes submitted to progressive drought and subsequent recovery. J Plant Physiol, 2010, 167(2): 114-120, DOI
21	Farooq M, Wahid A, Kobayashi N, Fujita D, Basra SMA. Plant drought stress: effects, mechanisms and management. Agron Sustain Dev, 2009, 29: 185-212, DOI
22	Feng W, Lindner H, Robbins NE, Dinneny JR. Growing out of stress: the role of cell- and organ-scale growth control in plant water-stress responses. Plant Cell, 2016, 28: 1769-1782, DOI
23	Ferchichi S, Hessini K, Dell'Aversana E, D'Amelia L, Woodrow P, Ciarmiello LF, Carillo P. Hordeum vulgare and Hordeum maritimum respond to extended salinity stress displaying different temporal accumulation pattern of metabolites. Funct Plant Biol, 2018, 45(11): 1096-1109, DOI
24	Furlan A, Bianucci E, del Carmen TM, Kleinert A, Valentine A, Castro S. Dynamic responses of photosynthesis and the antioxidant system during a drought and rehydration cycle in peanut plants. Func Plant Biol, 2016, 43: 337-345, DOI
25	Gupta A, Rico-Medina A, Caño-Delgado AI. The physiology of plant responses to drought. Science, 2020, 368: 266-269, DOI
26	Hageman RH, Hucklesby DP. Pietro AS. Nitrate reductase from higher plants. Methods in Enzymology, 1971 New York Academic Press 491-503
27	Hamouda I, Badri M, Mejri M, Cruz C, Siddique KHM, Hessini K. Salt tolerance of Beta macrocarpa is associated with efficient osmotic adjustment and increased apoplastic water content. Plant Biol, 2016, 18(3): 369-375, DOI
28	Hessini K, Ghandour M, Albouchi A, Soltani A, Koyro HW, Abdelley C. Biomass production, photosynthesis, and leaf water relations of Spartina alterniflora under moderate water stress. J Plant Res, 2008, 121: 311-318, DOI
29	Hessini K, Martinez JP, Gandour M, Albouchi A, Soltani A, Abdelly C. Effect of water stress on growth, osmotic adjustment, cell wall elasticity and water use efficiency in Spartina alterniflora. Environ Exp Bot, 2009, 67: 312-319, DOI
30	Hunt R. Plant growth analysis: Second derivatives and compounded second derivatives of splined plant growth curves. Ann Bot, 1982, 50: 317-328, DOI
31	Inskeep WP, Bloom PR. Extinction coefficients of chlorophyll a and b in N, N-Dimethylformamide and 80% acetone. Plant Physiol, 1985, 77: 483-485, DOI
32	IPCC (2013) Summary for policymakers, in climate change 2013: the physical science basis. Contribution of working group I to the Fifth assessment report of the intergovernmental panel on climate change, Stocker TF, Qin D, Plattner GK, Tignor M, Allen SK, Boschung J et al (eds.). Cambridge University Press, New York, 32p.
33	Jones HG, Corlett JE. Current topics in drought physiology. J Agr Sci, 1992, 119: 291-296, DOI
34	Kim JH, Lee-Stadelman OY. Water relations and cell wall elastic quantities in Phaseolus vulgaris leaves. J Exp Bot, 1984, 35: 841-858, DOI
35	Koide RT, Robert HR, Suzanne RM, Celia MS. Pearcy RW, Ehleringer JR, Mooney HA, Rundel PW. Plant water status, hydraulic resistance and capacitance. Plant physiological ecology; field methods and instrumentation, 1989 London Chapman and Hall 209-253
36	Lambers H, Chapin FS III, Pons T. Lambers H, Chapin Iii FS, Pons T. Plant water relations. Plant Physiological Ecology, 2008 New York Springer 163-223, DOI
37	Lamont BB, Lamont HC. Utilizable water in leaves of 8 arid species as derived from pressure–volume curves and chlorophyll fluorescence. Physiol Plant, 2000, 110: 64-71, DOI
38	Le Gall H, Philippe F, Domon JM, Gillet F, Pelloux J, Rayon C. Cell wall metabolism in response to abiotic stress. Plants, 2015, 4(1): 112-166, DOI
39	Lee YT, Langenheim JH. A systematic revision of the genus Hymenaea (Leguminosae; Caesalpinioideae; Detarieae). Univ Calif Publ Bot, 1975, 69: 1-109
40	Liu FH, Stützel H. Biomass partitioning, specific leaf area, and water use efficiency of vegetable amaranth (Amaranthus spp.) in response to water stress. Sci Hortic, 2004, 102: 15-27, DOI
41	Lorenzi H. Árvores brasileiras: manual de identificação e cultivo de plantas arbóreas nativas do Brasil, 2000 3 Nova Odessa Plantarum 352
42	MacKintosh C, Meek SEM. Regulation of plant NR activity by reversible phos-phorylation, 14–3-3 proteins and proteolysis. Cell Mol Life Sci, 2001, 58: 205-214, DOI
43	Marín-de la Rosa N, Lin CW, Kang YJ, Dhondt S, Gonzalez N, Inzé D, Falter-Braun P. Drought resistance is mediated by divergent strategies in closely related Brassicaceae. New Phytol, 2019, 223: 783-797, DOI
44	Martínez JP, Lutts S, Schanck A, Bajji M, Kinet JM. Is osmotic adjustment required for water stress resistance in the Mediterranean shrub (Atriplex halimus L.)?. J Plant Physiol, 2004, 161: 1041-1051, DOI
45	Martίnez JP, Silva H, Ledent JF, Pinto M. Effect of drought stress on the osmotic adjustment, cell wall elasticity and cell volume of six cultivars of common beans (Phaseolus vulgaris L.). Eur J Agron, 2007, 26: 30-38, DOI
46	McCarty GW, Bremner JM. Inhibition of assimilatory nitrate reductase-activity in soil by glutamine and ammonium analogs. Proc Natl Acad Sci, 1992, 89: 5834-5836, DOI
47	Meena YK, Kaur N. Towards an understanding of physiological and biochemical mechanisms of drought tolerance in plants. Annu Res Rev Biol, 2019, 31(2): 1-13, DOI
48	De Melo MGG, Mendes AMS (2005) Jatobá Hymenaea courbaril L. Informativo Técnico Rede de Sementes da Amazônia 9. Available on: https://www.inpa.gov.br/sementes/iT/9_Jatoba.pdf [accessed 20.05.2022]
49	Moore JP, Vicré-Gibouin M, Farrant JM, Driouich A. Adaptations of higher plant cell walls to water loss: drought vs desiccation. Physiol Plantarum, 2008, 134(2): 237-245, DOI
50	Moraes MLT, Moraes SMB, Polizeli MLTM, Sá ME, Sá AAB (2001) Composição química de sementes de jatobá (Hymenaea stigonocarpa). Informativo ABRATES 11(2), Londrina, 264 p.
51	NASA (2014) Global climate change: vital signs of the planet. Available on http://climate.nasa.gov/ [accessed May 05, 2022].
52	Nobel PS. Biophysical plant physiology and ecology, 1983 San Francisco WH Freeman 603
53	Nobre CA, Sampaio G, Borma LS, Castilla-Rubio JC, Silva JS, Cardoso M. Land-use and climate change risks in the Amazon and the need of a novel sustainable development paradigm. Proc Natl Acad Sci USA, 2016, 113: 10759-10768, DOI
54	Oaks A, Aslam M, Boesel I. Ammonium and amino acids as regulators of nitrate reductase in corn roots. Plant Physiol, 1977, 59(3): 391-394, DOI
55	Oliveira VB, Yamada LT, Fagg CW, Brandão MGL. Native foods from Brazilian biodiversity as a source of bioactive compounds. Food Res Intern, 2012, DOI
56	Peaucelle A, Braybrook S, Höfte H. Cell wall mechanics and growth control in plants: the role of pectins revisited. Front Plant Sci, 2012, 3: 1-6, DOI
57	Peoples MB, Faizah AW, Reakasem BE, Herridge DF. Methods for evaluating nitrogen fixation by nodulated legumes in the field, 1989 Canberra Australian Centre for International Agricultural Research 76
58	Pinto R, Lusa M, Mansano V, Tozzi A. Morphoanatomy of the leaflets of the Hymenaea clade (Fabaceae, Detarioideae) reveals their potential for taxonomic and phylogenetic studies. Bot J Linn, 2018, 187: 87-98, DOI
59	PRODES (2021) TerraBrasilis—Taxas anuais de desmatamento na Amazônia Legal Brasiliera. Available on http://www.dpi.inpe.br/prodesdigital/prodesmunicipal.php [accessed on April 4, 2022]
60	R Core Team. R: A language and environment for statistical computing, 2021 Vienna R Foundation for Statistical Computing
61	Robbins NE, Dinneny JR. The divining root: moisture-driven responses of roots at the micro- and macro-scale. J Exp Bot, 2015, 66: 2145-2154, DOI
62	Rui Y, Dinneny JR. A wall with integrity: surveillance and maintenance of the plant cell wall under stress. New Phytol, 2020, 225(4): 1428-1439, DOI
63	Sack L, Tyree M. Zwieniecki MA, Holbrook NM. Leaf hydraulics and its implications in plant structure and function. Vascular transport in plants, 2005 London Academic Press 93-114, DOI
64	Sanders GJ, Arndt SK. Aroca R. Osmotic adjustment under drought conditions. Plant responses to drought stress: from morphological to molecular features, 2012 Berlin Springer Verlag
65	Schwartz G. Jatoba - Hymenaea courbaril. Exot Fruits, 2018, DOI
66	Shtein I, Shelef Y, Marom Z, Zelinger E, Schwartz A, Popper ZA. Stomatal cell wall composition: distinctive structural patterns associated with different phylogenetic groups. Ann Bot, 2017, 119: 1021-1033, DOI
67	Silva AA, Fonseca GG. Brazilian savannah fruits: characteristics, properties and potential application. Food Sci Biotechnol, 2016, 25: 1225-1232, DOI
68	Slavick B. Methods of studying plant water relations, 1979 New York Springer Verlang 449p
69	Souza IM, Funch LS, Queiroz LP. Morphological analyses suggest a new taxonomic circumscription for Hymenaea courbaril L. (Leguminosae, Caesalpinioideae). PhytoKeys, 2014, 38: 101-118, DOI
70	Srivastava HS. Regulation of nitrate reductase activity in higher plants. Phytochemistry, 1980, 19: 725-733, DOI
71	Turner NC. Turgor maintenance by osmotic adjustment: 40 years of progress. J Exp Bot, 2018, 69(13): 3223-3233, DOI
72	Yanagisawa S. Transcription factors involved in controlling the expression of nitrate reductase genes in higher plant. Plant Sci, 2014, 229: 167-171, DOI