Abstract
Key message
PITOTAL, PIABS, DI0/RC, and δR0 are good markers of water stress in mango trees, demonstrating that consecutive drought cycles can develop differential acclimatization, depending on the rootstock used.
Abstract
Drought stress is one of the premier limitations to global agricultural production due to the complexity of the water-limiting environment and changing climate. In addition to indicating plant drought stress, photosynthetic performance is also determined by the scion/rootstock combination. The chlorophyll a fluorescence analysis is a reliable method to identify the most promising rootstock in the production of ‘Uba’ mango seedlings. We tested the hypothesis that different rootstocks can change the physiological responses related to chlorophyll a fluorescence, gas exchange, and proline content of different combinations of mango scion/rootstocks after three consecutive drought cycles, identifying the most vigorous rootstock with the ability to generate ‘Uba’ mango trees with greater differential resistance to drought. The Oleo rootstock (UC2/Oleo combination) has the greatest ability to imprint differential drought resistance in ‘Uba’ mango scions, generating plants with more vigor and better resistance to water deficit. The results suggest that the plant’s consecutive cycles of drought have been “learned” as a resistance mechanism to cope with severe water shortages in the future.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data availability
The generated and analyzed database for the current study is available from the corresponding author on reasonable request.
References
Abid M, Tian Z, Zahoor R, Ata-Ul-Karim ST, Daryl C, Snider JL, Dai T (2018) Pre-drought priming: a key drought tolerance engine in support of grain development in wheat. Advances in Agronomy. Elsevier Ltd., Amsterdam. https://doi.org/10.1016/bs.agron.2018.06.001
Alia, Mohanty P, Matysik J (2001) Effect of proline on the production of singlet oxygen. Amino Acids 21:195–200. https://doi.org/10.1007/s007260170026
Ashraf MA, Iqbal M, Rasheed R, Hussain I, Perveen S, Mahmood S (2018) Dynamic proline metabolism: importance and regulation in water-limited environments. In: Plant metabolites and regulation under environmental stress. Elsevier Inc., Amsterdam, pp 323–336. https://doi.org/10.1016/B978-0-12-812689-9.00016-9
Bates LS, Waldren RP, Teare ID (1973) Rapid determination of free proline for water-stress studies. Plant Soil 39:205–207. https://doi.org/10.1007/BF00018060
Bithell SL, Tran-Nguyen LTT, Hearnden MN, Hoult MD, Hartley N, Smith MW (2016) Fine root dry matter relative to mango (Mangifera indica) tree scion size grafted on size-controlling rootstocks, is negatively related to scion growth rate. Trees - Struct Funct 30:1181–1190. https://doi.org/10.1007/s00468-016-1355-z
Bratt A, Rosenwasser S, Meyer A, Fluhr R (2016) Organelle redox autonomy during environmental stress. Plant Cell Environ 39:1909–1919. https://doi.org/10.1111/pce.12746
Bruce TJA, Matthes MC, Napier JA, Pickett JA (2007) Stressful “memories” of plants: evidence and possible mechanisms. Plant Sci 173:603–608. https://doi.org/10.1016/j.plantsci.2007.09.002
Chadwick R, Good P, Martin G, Rowell DP (2015) Large rainfall changes consistently projected over substantial areas of tropical land. Nat Clim Change 6:177–181. https://doi.org/10.1038/nclimate2805
Challabathula D, Zhang Q, Bartels D (2018) Protection of photosynthesis in desiccation-tolerant resurrection plants. J Plant Physiol 227:84–92. https://doi.org/10.1016/j.jplph.2018.05.002
Czyczyło-Mysza I, Myśków B (2017) Analysis of the impact of drought on selected morphological, biochemical and physiological traits of rye inbred lines. Acta Physiol Plant 39:87. https://doi.org/10.1007/s11738-017-2385-x
Dayal V, Dubey AK, Singh SK, Sharma RM, Dahuja A, Kaur C (2016) Growth, yield and physiology of mango (Mangifera indica L.) cultivars as affected by polyembryonic rootstocks. Sci Hortic (amsterdam) 199:186–197. https://doi.org/10.1016/j.scienta.2015.12.042
de Freitas Guedes FA, Nobres P, Rodrigues Ferreira DC, Menezes-Silva PE, Ribeiro-Alves M, Correa RL, DaMatta FM, Alves-Ferreira M (2018) Transcriptional memory contributes to drought tolerance in coffee (Coffea canephora) plants. Environ Exp Bot 147:220–233. https://doi.org/10.1016/j.envexpbot.2017.12.004
Dumroese RK, Luna T, Landis TD (2009) Nursery manual for native plants a guide for tribal nurseries, vol 1. Nursery management, 1st edn, Agriculture Handbook 730. Department of Agriculture, Forest Service, Washington
Elsheery NI, Cao K-F (2008) Gas exchange, chlorophyll fluorescence, and osmotic adjustment in two mango cultivars under drought stress. Acta Physiol Plant 30:769–777. https://doi.org/10.1007/s11738-008-0179-x
Faria-Silva L, Gallon CZ, Filgueiras PR, Silva DM (2019) Irrigation improves plant vitality in specific stages of mango tree development according to photosynthetic efficiency. Photosynthetica 57:820–829. https://doi.org/10.32615/ps.2019.091
Faria-Silva L, Gallon CZ, Silva DM (2020a) Photosynthetic performance is determined by scion/rootstock combination in mango seedling propagation. Sci Hortic (amsterdam) 265:1–8. https://doi.org/10.1016/j.scienta.2020.109247
Faria-Silva L, Ventura JA, Silva DM (2020b) Registration of new mango cultivar “Óleo ES5003”. National Register of Cultivars (RNC) of the Ministry of Agriculture, Livestock and Supply (MAPA). Registration 44881. https://sistemas.agricultura.gov.br/snpc/cultivarweb/detalhe_cultivar.php?codsr=44842
Fleta-Soriano E, Munné-Bosch S (2016) Stress memory and the inevitable effects of drought: a physiological perspective. Front Plant Sci 7:1–6. https://doi.org/10.3389/fpls.2016.00143
Fleta-Soriano E, Pintó-Marijuan M, Munné-Bosch S (2015) Evidence of drought stress memory in the facultative CAM, Aptenia cordifolia: possible role of phytohormones. PLoS One 10:1–12. https://doi.org/10.1371/journal.pone.0135391
Gregory PJ, Atkinson CJ, Bengough AG, Else MA, Fernández-Fernández F, Harrison RJ, Schmidt S (2013) Contributions of roots and rootstocks to sustainable, intensified crop production. J Exp Bot 64:1209–1222. https://doi.org/10.1093/jxb/ers385
Guan XK, Song L, Wang TC, Turner NC, Li FM (2014) Effect of drought on the gas exchange, chlorophyll fluorescence and yield of six different-era spring wheat cultivars. J Agron Crop Sci 201:253–266. https://doi.org/10.1111/jac.12103
Guha A, Sengupta D, Reddy AR (2013) Polyphasic chlorophyll a fluorescence kinetics and leaf protein analyses to track dynamics of photosynthetic performance in mulberry during progressive drought. J Photochem Photobiol B Biol 119:71–83. https://doi.org/10.1016/j.jphotobiol.2012.12.006
Hare PD, Cress WA, Van Staden J (1999) Proline synthesis and degradation: a model system for elucidating stress-related signal transduction. J Exp Bot 50:413–434. https://doi.org/10.1093/jxb/50.333.413
Hubbard RM, Ryan MG, Stiller V, Sperry JS (2001) Stomatal conductance and photosynthesis vary linearly with plant hydraulic conductance in ponderosa pine. Plant Cell Environ 24:113–121. https://doi.org/10.1046/j.1365-3040.2001.00660.x
Iwasaki M, Paszkowski J (2014) Epigenetic memory in plants. EMBO J 33:1987–1998. https://doi.org/10.15252/embj.201488883
Karimi HR, Beniaz N, Mohammadi Mirik AA (2019) Effects of rootstock on growth indices and echo physiological parameters of scion pomegranate. Int J Fruit Sci 19:326–346. https://doi.org/10.1080/15538362.2018.1563761
Kinoshita T, Seki M (2014) Epigenetic memory for stress response and adaptation in plants. Plant Cell Physiol 55:1859–1863. https://doi.org/10.1093/pcp/pcu125
Li SY, Wang WB, Yao XD, Wang CL, Cao YQ, Zhang LJ, Zhang HJ, Xie FT, Song SH (2019) Photosynthesis in reciprocal grafts of drought-tolerant and drought- sensitive cultivars of soybean under water stress. Photosynthetica 57:942–949. https://doi.org/10.32615/ps.2019.109
Li Y, Xu W, Ren B, Zhao B, Zhang J, Liu P, Zhang Z (2020) High temperature reduces photosynthesis in maize leaves by damaging chloroplast ultrastructure and photosystem II. J Agron Crop Sci 00:1–17. https://doi.org/10.1111/jac.12401
Liu L, Kon H, Matsuoka N, Kobayashi T (2005) Coordination between stomatal conductance and leaf-specific hydraulic conductance in maize (Zea mays L.). J Agric Meteorol 61:143–152. https://doi.org/10.2480/agrmet.61.143
Liu CC, Liu YG, Guo K, Zheng YR, Li GQ, Yu LF, Yang R (2010) Influence of drought intensity on the response of six woody karst species subjected to successive cycles of drought and rewatering. Physiol Plant 139:39–54. https://doi.org/10.1111/j.1399-3054.2009.01341.x
Liu B, Liang J, Tang G, Wang X, Liu F, Zhao D (2019) Drought stress affects on growth, water use efficiency, gas exchange and chlorophyll fluorescence of Juglans rootstocks. Sci Hortic (amsterdam) 250:230–235. https://doi.org/10.1016/j.scienta.2019.02.056
Losciale P, Manfrini L, Morandi B, Pierpaoli E, Zibordi M, Stellacci AM, Salvati L, Corelli Grappadelli L (2015) A multivariate approach for assessing leaf photo-assimilation performance using the I PL index. Physiol Plant 154:609–620. https://doi.org/10.1111/ppl.12328
Martínez-Ballesta MC, Alcaraz-López C, Muries B, Mota-Cadenas C, Carvajal M (2010) Physiological aspects of rootstock-scion interactions. Sci Hortic (amsterdam) 127:112–118. https://doi.org/10.1016/j.scienta.2010.08.002
Mashilo J, Odindo AO, Shimelis HA, Musenge P, Tesfay SZ, Magwaza LS (2017) Drought tolerance of selected bottle gourd [Lagenaria siceraria (Molina) Standl.] landraces assessed by leaf gas exchange and photosynthetic efficiency. Plant Physiol Biochem 120:75–87. https://doi.org/10.1016/j.plaphy.2017.09.022
Mendanha T, Rosenqvist E, Nordentoft Hyldgaard B, Doonan JH, Ottosen C (2020) Drought priming effects on alleviating the photosynthetic limitations of wheat cultivars (Triticum aestivum L.) with contrasting tolerance to abiotic stresses. J Agron Crop Sci. https://doi.org/10.1111/jac.12404
Menezes-Silva PE, Sanglard LMVP, Ávila RT, Morais LE, Martins SCV, Nobres P, Patreze CM, Ferreira MA, Araújo WL, Fernie AR, DaMatta FM (2017) Photosynthetic and metabolic acclimation to repeated drought events play key roles in drought tolerance in coffee. J Exp Bot 68:4309–4322. https://doi.org/10.1093/jxb/erx211
Mukherjee S, Chakraborty A, Mondal S, Saha S, Haque A, Paul S (2019) Assessment of common plant parameters as biomarkers of air pollution. Environ Monit Assess 191:400. https://doi.org/10.1007/s10661-019-7540-y
Munday JC, Govindjee (1969) Light-induced changes in the fluorescence yield of chlorophyll a in vivo: III. The dip and the peak in the fluorescence transient of Chlorella pyrenoidosa. Biophys J 9:1–21. https://doi.org/10.1016/S0006-3495(69)86365-4
Murchie EH, Lawson T (2013) Chlorophyll fluorescence analysis: a guide to good practice and understanding some new applications. J Exp Bot 64:3983–3998. https://doi.org/10.1093/jxb/ert208
Neves DM, Santana-Vieira DDS, Dória MS, Freschi L, Ferreira CF, dos Soares Filho WS, Costa MGC, CoelhoFilho MA, Micheli F, da Gesteira AS (2018) Recurrent water deficit causes alterations in the profile of redox proteins in citrus plants. Plant Physiol Biochem 132:497–507. https://doi.org/10.1016/j.plaphy.2018.09.035
Niinemets Ü, Bilger W, Kull O, Tenhunen JD (1999) Responses of foliar photosynthetic electron transport, pigment stoichiometry, and stomatal conductance to interacting environmental factors in a mixed species forest canopy. Tree Physiol 19:839–852. https://doi.org/10.1093/treephys/19.13.839
Nowicka B, Ciura J, Szymańska R, Kruk J (2018) Improving photosynthesis, plant productivity and abiotic stress tolerance—current trends and future perspectives. J Plant Physiol 231:415–433. https://doi.org/10.1016/j.jplph.2018.10.022
Obiero CO, Milroy SP, Bell RW (2020) Photosynthetic and respiratory response of potato leaves of different ages during and after an episode of high temperature. J Agron Crop Sci. https://doi.org/10.1111/jac.12391
Pommerening A, Grabarnik P (2019) Principles of relative growth analysis. In: Individual-based methods in forest ecology and management. Springer International Publishing, Cham, pp 253–301. https://doi.org/10.1007/978-3-030-24528-3_6
Ptushenko OS, Ptushenko VV (2019) Tradescantia-based models: a powerful looking glass for investigation of photoacclimation and photoadaptation in plants. Physiol Plant 166:120–133. https://doi.org/10.1111/ppl.12963
Ribeiro IJA, Rosseto CJ, Donadio AC, Sabino JC, Martins ALM, Gallo PB (1995) Mango wilt. XIV Selection of mango (Mangifera indica L.) rootstocks resistant to the mango wilt fungus Ceratocystis fimbriata. In: Acta Horticulturae. International symposium on tropical, pp 159–166
Smith JB, Schellnhuber HJ, Mirza MMQ (2001) Vulnerability to climate change and reasons for concern: a synthesis. In: McCarthy JJ, Canziani OF, Leary NA, Dokken DJ, White KS (eds) Climate change 2001: impacts, adaptation, and vulnerability. Cambridge University Press, Cambridge, pp 913–967
Smith MW, Hoult MD, Bright JD (2003) Rootstock affects yield, yield efficiency, and harvest rate of “Kensington Pride” mango. HortScience 38:273–276. https://doi.org/10.21273/hortsci.38.2.273
Stirbet A, Govindjee (2011) On the relation between the Kautsky effect (chlorophyll a fluorescence induction) and Photosystem II: basics and applications of the OJIP fluorescence transient. J Photochem Photobiol B Biol 104:236–257. https://doi.org/10.1016/j.jphotobiol.2010.12.010
Stirbet A, Lazár D, Kromdijk J, Govindjee (2018) Chlorophyll a fluorescence induction: can just a one-second measurement be used to quantify abiotic stress responses? Photosynthetica 56:1–19. https://doi.org/10.1007/s11099-018-0770-3
Strasser RJ, Srivastava A, Govindjee (1995) Polyphasic chlorophyll a fluorescence transient in plants and cyanobacteria. Photochem Photobiol 61:32–42. https://doi.org/10.1111/j.1751-1097.1995.tb09240.x
Strasser RJ, Tsimilli-Michael M, Srivastava A (2004) Analysis of the chlorophyll a fluorescence transient. In: Papageorgiou GC, Govindjee (eds) Chlorophyll a fluorescence: a signature of photosynthesis. Springer Netherlands, Dordrecht, pp 321–362. https://doi.org/10.1007/978-1-4020-3218-9_12
Tombesi S, Frioni T, Poni S, Palliotti A (2018) Effect of water stress “memory” on plant behavior during subsequent drought stress. Environ Exp Bot. https://doi.org/10.1016/j.envexpbot.2018.03.009
Urban L, Aarrouf J, Bidel LPR (2017) Assessing the effects of water deficit on photosynthesis using parameters derived from measurements of leaf gas exchange and of chlorophyll a fluorescence. Front Plant Sci 8:1–18. https://doi.org/10.3389/fpls.2017.02068
Walter J, Nagy L, Hein R, Rascher U, Beierkuhnlein C, Willner E, Jentsch A (2011) Do plants remember drought? Hints towards a drought-memory in grasses. Environ Exp Bot 71:34–40. https://doi.org/10.1016/j.envexpbot.2010.10.020
Yamori W, Shikanai T (2016) Physiological functions of cyclic electron transport around photosystem I in sustaining photosynthesis and plant growth. Annu Rev Plant Biol 67:81–106. https://doi.org/10.1146/annurev-arplant-043015-112002
Zaharah SS, Razi IM (2009) Growth, stomata aperture, biochemical changes and branch anatomy in mango (Mangifera indica) cv. Chokanan in response to root restriction and waterstress. Sci Hortic (amsterdam) 123:58–67. https://doi.org/10.1016/j.scienta.2009.07.022
Zhou Y, Tian X, Yao J, Zhang Z, Wang Y, Zhang X, Li W, Wu T, Han Z, Xu X, Qiu C (2020) Morphological and photosynthetic responses differ among eight apple scion-rootstock combinations. Sci Hortic (amsterdam) 261:108981. https://doi.org/10.1016/j.scienta.2019.108981
Acknowledgements
We thank the National Council for Scientific and Technological Development (CNPq, Brazil) for supporting this research and the nursery Frucafé Mudas e Plantas Ltda. and Mr. Erli Ropke for material support.
Funding
This study was financed in part by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior—Brasil (CAPES)—Finance Code 001.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Fig. S1
Relationships between net photosynthesis (µmol CO2 m−2 s−1) with drought days (A, B, C) and substrate moisture content with drought days (D, E, F) in pots with UC2/Oleo (A, D), UC2/Uba (B, E) and UC2/Imbu (C, F) combinations. The substrate moisture content was represented by a HydroFarm portable meter (%) and by the calculated volumetric substrate moisture content (VSMC), i.e., H2O content (cm−3) per substrate total volume (cm−3). Error bars represent ± SE of the mean (n = 3) (TIF 20182 KB)
Fig. S2
Relationship between substrate moisture calculated by volumetric substrate moisture content (VSMC, cm−3 cm−3) and measured by HydroFarm apparatus (%) (TIF 9641 KB)
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Faria-Silva, L., Silva, D.M. Different rootstocks can change the photosynthetic performance of the ‘Uba’ mango scion after recurrent drought events. Trees 37, 1385–1399 (2023). https://doi.org/10.1007/s00468-023-02429-x
Received:
Accepted:
Published:
Version of record:
Issue date:
DOI: https://doi.org/10.1007/s00468-023-02429-x