Abstract
Key message
Progressive drought induced a gradual increase in non-structural carbohydrates in roots and leaves, slowing the drop in water status. The roots had an increase of 95 % compared to well-watered plants, while the leaves only increased by 21 %. Since Cenostigma pyramidale is a deciduous species, the non-structural carbohydrates are mainly found in the roots, which helps the plant survive the intense drought period.
Abstract
The ability to produce and control the distribution of non-structural carbohydrates (NSC) may be critical to the success of deciduous woody plants from seasonally dry tropical forests. Thus, our aim was to investigate how carbohydrate allocation occurs and the dynamics of water status during the pre-senescence leaf period. We performed a controlled experiment on progressive drought stress using Cenostigma pyramidale, and found that leaf relative water content decreased only under severe drought conditions (SVD), when soil water content was approximately 5%, three times less than well-hydrated plants, and foliar relative water content (RWC) was close to 35%. Gas exchange was maintained at a high level until the moderate drought stage (MD), with soil water content and RWC of 8% and 75%, respectively. Prior to leaf senescence, C. pyramidale maintained the net CO2 assimilation and intense production of NSC, which were stored mainly in the leaves (45%), and roots (44%), with only 11% in the stems. This increase in root NSC content during progressive drought levels suggests that this tissue may be the main storage site for NSC, which could allow the plant to survive the dry season, and also have reserves for leaf sprouting at the beginning of the next rainy season. The results suggest that studies involving carbon metabolism in woody species under stress should consider root tissue, as this is an important source of NSC during drought.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Allen CD, Macalady AK, Chenchouni H, Bachelet D, McDowell N et al (2010) A global overview of drought and heat-induced tree mortality reveals emerging climate change risks for forests. For Ecol Manag 259:660–684. https://doi.org/10.1016/j.foreco.2009.09.001
Barrs HD, Weatherley PE (1962) A re-examination of the relative turgidity technique for estimating water deficits in leaves. Aust J Biol Sci 15:413–428. https://doi.org/10.1071/BI9620413
Basu S, Ramegowda V, Kumar A, Pereira A (2016) Plant adaptation to drought stress. Crop Soil Environ Sci 1554:1–10. https://doi.org/10.12688/f1000research.7678.1
Brunner I, Herzog C, Dawes MA, Arend M, Sperisen C (2015) How tree roots respond to drought. Front Plant Sci 6:547. https://doi.org/10.3389/fpls.2015.00547
Campbell G, Norman J (1998) An introduction to environmental biophysics, 2nd edn. Springer, New York
Chaves MM et al (2016) Controlling stomatal aperture in semi-arid regions-—the dilemma of saving water or being cool? Plant Sci 251:54–64. https://doi.org/10.1016/j.plantsci.2016.06.015
Chazdon RL, Broadbent EN, Rozendaal DMA, Bongers F, Zambrano AMA et al (2016) Carbon sequestration potential of second-growth forest regeneration in the Latin American tropics. Science 2:1–10. https://doi.org/10.1126/sciadv.1501639
Dietze MS, Sala N, Carbone MS, Czimczik CI, Mantooth J, Richardson AD, Vargas R (2014) Nonstructural carbon in woody plants. Annu Rev Plant Biol 65:667–687. https://doi.org/10.1146/annurev-arplant-050213-040054
Dubois M, Gilles K, Hamilton J, Rebers P, Smith F (1956) Colorimetric method for determination of sugars and related substances. Anal Chem 28:350–356. https://doi.org/10.1021/ac60111a017
Eveland AL, Jackson DP (2012) Sugars, signalling, and plant development. J Exp Bot 63:3367–3377. https://doi.org/10.1093/jxb/err379
Falcão HM, Mdeiros CD, Silva BLR, Sampaio EVSB, Almeida-Cortez JS, Santos MG (2015) Phenotypic plasticity and ecophysiological strategies in a tropical dry forest chronosequence: a study case with Poincianella pyramidalis. For Ecol Manag 340:62–69. https://doi.org/10.1016/j.foreco.2014.12.029
Frosi G, Barros VA, Oliveira MT, Santos M, Ramos DG, Maia LC, Guida MS (2016) Symbiosis with AMF and leaf Pi supply increases water déficit tolerance of woody species form seasonal dru tropical forest. J Plant Physiol 207:84–93. https://doi.org/10.1016/j.jplph.2016.11.002
Frosi G, Harand W, Oliveira MT, Pereira S, Cabral SP, Montenegro AAA, Santos MG (2017) Different physiological responses under drought stress result in different recovery abilities of two tropical woody evergreen species. Acta Bot Bras 31:153–160. https://doi.org/10.1016/j.jplph.2016.11.002
Hagedorn F, Joseph J, Peter M et al (2016) Recovery of trees from drought depends on belowground sink control. Nature 2:1–5. https://doi.org/10.1038/NPLANTS.2016.111
Hartmann H, Ziegler W, Trumbore S (2013) Lethal drought leads to reduction in nonstructural carbohydrates in Norway spruce tree roots but not in the canopy. Funct Ecol 27:413–427. https://doi.org/10.1111/1365-2435.12046
Hartmann H, Adamsb HD, Hammondb WM, Hochc G, Landhäusserd SM, Wileyd E, Zaehlea S (2018) Identifying differences in carbohydrate dynamics of seedlings and mature trees to improve carbon allocation in models for trees and forests. Environ Exp Bot 152:7–18. https://doi.org/10.1016/j.envexpbot.2018.03.011
Hattmann H, Trumbore S (2016) Understanding the roles of nonstructural carbohydrates in forest trees—from what wecan measure to what we want to know. New Phytol 211:386–403. https://doi.org/10.1111/nph.13955
Hsiao TC (1973) Plant responses to water stress. Annu Rev Plant Physiol 24:519–570. https://doi.org/10.1146/annurev.pp.24.060173.002511
Lima ALA, Sampaio EVSB, Castro CC, Rodal MJN, Antonino ACD, Melo AL (2012) Do the phenology and functional stem attributes of woody species allow for the identification of functional groups in the semiarid region of Brazil? Trees 26:1605–1616. https://doi.org/10.1007/s00468-012-0735-2
Marengo JA, Bernasconi A (2015) Regional differences in aridity/drought conditions over Northeast Brazil: present state and future projections. Clim Change 129:103–115. https://doi.org/10.1007/s10584-014-1310-1
McDowell N et al (2008) Mechanisms of plant survival and mortality during drought: why do some plants survive while others succumb to drought? New Phytol 178:719–739. https://doi.org/10.1093/treephys/22.11.763
McDowell NG (2011) Mechanisms linking drought, hydraulics, carbon metabolism, and vegetation mortality. Plant Physiol 155:1051–1059. https://doi.org/10.1104/pp.110.170704
McDowell NG, Sevanto S (2010) The mechanisms of carbon starvation: how, when, or does it even occur at all? New Phytol 186:264–266. https://doi.org/10.1111/j.1469-8137.2010.03232.x
Mundim FM, Pringle EG (2018) Whole plant metabolic allocation under water stress. Front Plant Sci 9:1–12. https://doi.org/10.3389/fpls.2018.00852
Nardini A, Casolo V, Borgo AD, Savi T, Stenni B, Betoncin P, Zini L, McDowell NG (2016) Rooting depth, water relations and non-structural carbohydrate dynamics in three woody angiosperms differentially affected by an extreme summer drought. Plant Cell Environ 39:618–627. https://doi.org/10.1111/pce.12646
Oliveira MT, Medeiros CD, Frosi G, Santos MG (2014) Different mechanisms drive the performance of native and invasive woody species in response to leaf phosphorus supply during periods of drought stress and recovery. Plant Physiol Biochem 82:66–75. https://doi.org/10.1016/j.plaphy.2014.05.006
Parker JD, Salminem JP, Agrawal AA (2012) Evolutionary potential of root chemical defense: genetic correlations with shoot chemistry and plant growth. J Chem Ecol 38:992–995. https://doi.org/10.1007/s10886-012-0163-1
Piper FI (2011) Drought induces opposite changes in the concentration of non-structural carbohydrates of two evergreen Nothofagus species of differential drought resistance. Ann For Sci 68:415–424. https://doi.org/10.1007/s13595-011-0030-1
Regier N, Streb S, Cocozza C, Schaub M, Cherubini P, Zeeman SC, Frey B (2009) Drought tolerance of two black poplar (Populus nigra L.) clones: contribution of carbohydrates and oxidative stress defence. Plant Cell Environ 32:1724–1736. https://doi.org/10.1111/j.1365-3040.2009.02030.x
Rivas R, Oliveira MT, Santos MG (2013) Three cycles of water deficit from seed to young plants of Moringa oleifera woody species improves stress tolerance. Plant Physiol Biochem 63:200–208. https://doi.org/10.1016/j.plaphy.2012.11.026
Rolland F, Baena-Gonzalez E, Sheen J (2006) Sugar sensing and signaling in plants: conserved and novel mechanisms. Annu Rev Plant Biol 57:675–709. https://doi.org/10.1146/annurev.arplant.57.032905.105441
Sala A, Piper IF, Hoch G (2010) Physiological mechanisms of drought-induced tree mortality are far from being resolved. New Phytol 186:274–281. https://doi.org/10.1111/j.1469-8137.2009.03167.x
Sala A, Woodruff DR, Meinzer FC (2012) Carbon dynamics in trees: feast or famine? Tree Physiol 32:764–775. https://doi.org/10.1093/treephys/tpr143
Santos MG, Oliveira MT, Figueiredo KV, Falcão H, Arruda E et al (2014) Caatinga, the Brazilian dry tropical forest: can it tolerate climate changes? Theor Exp Plant Physiol 26:83–99. https://doi.org/10.1007/s40626-014-0008-0
Secchi F, Zwieniecki MA (2011) Sensing embolism in xylem vessels: the role of sucrose as a trigger for refilling. Plant Cell Environ 34:514–524. https://doi.org/10.1111/j.1365-3040.2010.02259.x
Sevanto S, McDowell NG, Dickman LT, Pangle R, Pockman WT (2014) Plant Cell Enron 37:153–161. https://doi.org/10.1111/pce.12141
Souden S, Ennajeh M, Ouledali S, Massaudi N, Cochard H, Khemira H (2020) Water relations, photosynthesis, xylem embolism and accumulation of carbohydrates and cyclitols in two Eucalyptus species (E. camaldulensis and E. torquata) subjected to dehydration–rehydration cycle. Trees 34:1439–1452. https://doi.org/10.1007/s00468-020-02016-4
Tomasella M, Petrussa E, Petruzzellis F et al (2020) The possible role of nonstructural carbohydrates in the regulation of tree hydraulics. Int J Mol Sci 21:144. https://doi.org/10.3390/ijms21010144
Trugman AT, Detto M, Bartlett MK, Medvigy D, Anderegg, Schwalm C, Schaffer B, Pacala SW (2018) Tree carbon allocation explains forest drought-kill and recovery patterns. Ecol Lett 10:1552–1560. https://doi.org/10.1111/ele.13136
Wan X, Landhäusser SM, Liefers VJ, Zwiazek JJ (2006) Signals controlling root suckering and adventitious shoot formation in aspen (Populus tremuloides). Tree Physiol 26:681–687. https://doi.org/10.1093/treephys/26.5.681
Weemstra M, Mommer L, Visser EJW, Van Ruijven J, Kuyper TW, Mohren GMJ et al (2016) Towards a multidimensional root trait framework: a tree root review. New Phytol 211:1159–1169. https://doi.org/10.1111/nph.14003
Wiley E, Huepenbecker S, Casper BB, Helliker BR (2013) The effects of defoliation on carbon allocation: can carbon limitation reduce growth in favour of storage? Tree Physiol 33:1216–1228. https://doi.org/10.1093/treephys/tpt093
Williams AP, Allen CD, Macalady AK et al (2013) Temperature as a potent driver of regional forest drought stress and tree mortality. Nat Clim Change 3:292–297. https://doi.org/10.1038/NCLIMATE1693
Zhang T, Cao Y, Chen Y, Liu G (2015) Non-structural carbohydrate dynamics in Robinia pseudoacacia saplings under three levels of continuous drought stress. Trees 29:1837–1849. https://doi.org/10.1007/s00468-015-1265-5
Acknowledgements
This work was supported by Fundação de Amparo à Ciência e Tecnologia do Estado de Pernambuco (APQ/PRONEM-FACEPE-0336-2.03/14). This study was financed in part by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior—Brazil (CAPES)—Finance Code 001 for Mariana Santos scholarship. M.G.S. acknowledges CNPq for the fellowship granted.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Additional information
Victor Resco de Dios .
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Santos, M., Barros, V., Lima, L. et al. Whole plant water status and non‐structural carbohydrates under progressive drought in a Caatinga deciduous woody species. Trees 35, 1257–1266 (2021). https://doi.org/10.1007/s00468-021-02113-y
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00468-021-02113-y