Abstract
The plant breeding programs (PBP) of coffee plants (Coffea arabica L.) are always looking for new genotypes that perform better under water deficit. The ability of coffee trees responding to water stress is important for drought tolerance. In the search for drought tolerance strategies of promising genotypes in the PBP of the Empresa de Pesquisa Agropecuária de Minas Gerais (EPAMIG), young plants of two genotypes [07 and 19] were compared with two commercial cultivars [Catiguá MG3 and Catuaí Vermelho IAC 144] challenged to drought, followed by rehydration. By integrating results of xylem water potential and response curves of photosynthesis to CO2 and light with root anatomy, it was possible to identify the drought tolerance strategy of the new genotypes. Under water deficit conditions, the genotype 07 showed an increase in the number of root hairs and reductions in the root cross-section area, cortex thickness and tracheary element diameter, whereas genotype 19 showed an increase in the vascular cylinder area, in number of metaxylem poles and in number of tracheary elements. Despite the reduction of photosynthetic parameters under water deficit, the genotypes 07 and 19 showed higher values of maximum CO2 assimilation after the rehydration period. The drought tolerance in genotypes 07 and 19 was induced by a greater root plasticity, which increased hydraulic conductivity under water deficit, contributing to the restoration of photosynthetic efficiency after the return of water availability.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Aguiar ATE, Guerreiro-Filho O, Maluf MP, Gallo PB, Fazuoli LC (2004) Caracterização de cultivares de Coffea arabica mediante utilização de descritores mínimos. Bragantia 63:179–192. https://doi.org/10.1590/S0006-87052004000200003
Batista LA, Guimarães RJ, Pereira FJ, Carvalho GR, Castro EM (2010) Anatomia foliar e potencial hídrico na tolerância de cultivares de café ao estresse hídrico. Rev Ciênc Agron 41:475–481. https://doi.org/10.1590/S1806-66902010000300022
Begg JE, Turner NC (1970) Water potential gradients in field tobacco. Plant Physiol 46:343–346. https://doi.org/10.1104/pp.46.2.343
Bernacchi CJ, Singsaas EL, Pimentel C, Portis AR Jr, Long SP (2001) Improved temperature response functions for models of Rubisco-limited photosythesis. Plant Cell Environ 24:253–259. https://doi.org/10.1111/j.1365-3040.2001.00668.x
Cai ZQ, Chen Y-J, Guo Y-H, Cao K-F (2005) Responses of two field-grown coffee species to drought and re-hydration. Photosynthetica 43:187–193. https://doi.org/10.1007/s11099-005-0032-z
Cavatte PC, Oliveira AAG, Morais LE, Martins SCV, Sanglard LMVP, DaMatta FM (2012) Could shading reduce the negative impacts of drought on coffee? A morphophysiological analysis. Physiol Plant 144:111–122. https://doi.org/10.1111/j.1399-3054.2011.01525.x
Choné X, Leeuwen CV, Dubourdieu D, Gaudillère JP (2001) Stem water potential is a sensitive indicator of grapevine water status. Ann Bot 87:477–483. https://doi.org/10.1006/anbo.2000.1361
Cunha APMA, Zer M, Leal KD, Costa L, Cuartas LA, Marengo JA, Tomasella J, Vieira RM, Barbosa AA, Cunningham C, Garcia JVC, Broedel E, Alvalá R, Ribeiro-Neto G (2019) Extreme drought events over Brazil from 2011 to 2019. Atmosphere 10:642. https://doi.org/10.3390/atmos10110642
DaMatta FM, Maestri M, Barros RS, Regazzi AJ (1993) Water relations of coffee leaves (Coffea arabica and C. canephora) in response to drought. J Hortic Sci 68:741–746. https://doi.org/10.1080/00221589.1993.11516407
DaMatta FM, Maestri M, Mosquim PR, Barros RS (1997) Photosynthesis in coffee (Coffea arabica and C. canephora) as affected by winter and summer conditions. Plant Sci 128:43–50. https://doi.org/10.1016/S0168-9452(97)00142-8
DaMatta FM, Loos RA, Silva EA, Loureiro ME, Ducatti C (2002) Effects of soil water deficit and nitrogen nutrition on water relations and photosynthesis of pot-grown Coffea canephora Pierre. Trees 16:555–558. https://doi.org/10.1007/s00468-002-0205-3
DaMatta FM, Ronchi CP, Maestri M, Barros RS (2007) Ecophysiology of coffee growth and production. Braz J Plant Physiol 19:485–510. https://doi.org/10.1590/S1677-04202007000400014
DaMatta FM, Grandis A, Arenque BC, Buckeridge MS (2010) Impacts of climate changes on crop physiology and food quality. Food Res Int 43:1814–1823. https://doi.org/10.1016/j.foodres.2009.11.001
DaMatta FM, Godoy AG, Menezes-Silva PE, Martins SCV, Sanglard LMVP, Morais LE, Torre-Neto A, Ghini R (2016) Sustained enhancement of photosynthesis in coffee trees grown under free-air CO2 enrichment conditions: disentangling the contributions of stomatal, mesophyll, and biochemical limitations. J Exp Bot 67:341–352. https://doi.org/10.1093/jxb/erv463
DaMatta FM, Avila RT, Cardoso AA, Martins SCV, Ramalho JC (2018) Physiological and agronomic performance of the coffee crop in the context of climate change and global warming: a review. J Agric Food Chem 66:5264–5274. https://doi.org/10.1021/acs.jafc.7b04537
Deuner S, Alves JD, Zanandrea I, Goulart PFP, Silveira NM, Henrique PC, Mesquita AC (2011) Stomatal behavior and components of the antioxidative system in coffee plants under water stress. Sci Agric 68:77–85. https://doi.org/10.1590/S0103-90162011000100012
Empresa de Pesquisa Agropecuária de Minas Gerais—EPAMIG (2018) Cultivares de Café. Programa de Melhoramento Genético EPAMIG, EMBRAPA Café, UFV e UFLA. Ciência Móvel EPAMIG. http://www.sapc.embrapa.br/arquivos/consorcio/publicacoes_tecnicas/EPAMIG_Cultivares_Cafe.pdf. Accessed 31 July 2020
Fazuoli LC, Carvalho CHS, Carvalho GR, Filho OG, Pereira AA, Almeida SR, Matiello JB, Bartholo GF, Sera T, Moura WM, Mendes ANG, Fonseca AFA, Ferrão MAG, Ferrão RG, Nacif AP, Silvarolla MB (2007) Cultivares de café arábica (Coffea arabica L.). In: Carvalho CHS (ed) Cultivares de café. Brasília: EMBRAPA, pp 247
Ferrão RG, Moreira SO, Ferrão MAG, Riva EM, Arantes LO, Costa AFS, Carvalho PLPT, Galvêas PAO (2016) Genética e melhoramento: desenvolvimento e recomendação de cultivares com tolerância a seca para o Espírito Santo. Incaper Em Revista 6(7):51–71
Ferreira DF (2014) Sisvar: a guide for its bootstrap procedures in multiple comparisons. Ciênc Agrotec 38:109–112. https://doi.org/10.1590/S1413-70542014000200001
Fox J, Weisberg S (2019). An {R} companion to applied regression, third edition. Thousand Oaks CA: Sage. https://socialsciences.mcmaster.ca/jfox/Books/Companion/. Accessed 25 January 2021
Hazman M, Brown KM (2018) Progressive drought alters architectural and anatomical traits of rice roots. Rice 11:1–16. https://doi.org/10.1186/s12284-018-0252-z
Ilyas M, Nisar M, Khan N, Hazrat A, Khan AH, Hayat K, Fahad S, Khan A, Ullah A (2021) Drought tolerance strategies in plants: a mechanistic approach. J Plant Growth Regul 40:926–944. https://doi.org/10.1007/s00344-020-10174-5
Johansen DA (1940) Plant microtechnique. MacGraw-Hill Book, New York, p 523p
Kanechi M, Uchida NU, Yasuda T, Yamaguchi T (1988) Relationships between leaf water potential and photosynthesis of Coffea arabica L. grown under various environmental conditions as affected by withholding irrigation and re-irrigation. Jpn J Trop Agric 32:16–21. https://doi.org/10.11248/jsta1957.32.16
Kirschbaum MUF (2011) Does enhanced photosynthesis enhance growth? Lessons learned from CO2 enrichment studies. Plant Physiol 155:117–124. https://doi.org/10.1104/pp.110.166819
Köppen W (1948) Climatologia: con um estúdio de lós climas de la tierra. Fondo de Cultura Econômica. México, pp 479
Kraus JE, Arduin M (1997) Manual básico de métodos em morfologia vegetal. Seropédia, Edeir, pp 198
Lawlor DW (2002) Limitation to photosynthesis in water-stressed leaves: stomata vs. metabolism and the role of ATP. Ann Bot 89:871–885. https://doi.org/10.1093/aob/mcf110
Lawlor DW, Tezara W (2009) Causes of decreased photosynthetic rate and metabolic capacity in water-deficient leaf cells: a critical evaluation of mechanisms and integration of process. Ann Bot 103(561–579):124. https://doi.org/10.1093/aob/mcn244
Levitt J (1980) Responses of plants to environmental stress. In: Levitt J (ed) Water, radiation, salt, and other stress, 2d edn. Academic Press, New York, p 339p
Luo LJ (2010) Breeding for water-saving and drought-resistance rice (WDR) in China. J Exp Bot 61:3509–3517. https://doi.org/10.1093/jxb/erq185
Marchiori PER, Machado EC, Sales CRG, Espinoza-Núñez E, Magalhães Filho JR, Souza GM, Pires RCM, Ribeiro RV (2017) Physiological plasticity is important for maintaining sugarcane growth under water deficit. Front Plant Sci 8:1–12. https://doi.org/10.3389/fpls.2017.02148
Marshall B, Biscoe PV (1980) A model for C3 leaves describing the dependence of net photosynthesis on irradiance: II. application to the analysis of flag leaf photosynthesis. J Exp Bot 31:41–48. https://doi.org/10.1093/jxb/31.1.41
Martins SCV, Detmann KC, Reis JV, Pereira LF, Sanglard LMVP, Rogalski M, DaMatta FM (2013) Photosynthetic induction and activity of enzymes related to carbon metabolism: insights into the varying net phtosynthesis rates of coffee sun and shade leaves. Theor Exp Plant Physiol 25:62–69. https://doi.org/10.1590/S2197-00252013000100008
Martins SCV, Galmés J, Cavatte PC, Pereira LF, Ventrella MC, DaMatta FM (2014) Understanding the low photosynthetic rates of sun and shade coffee leaves: Bridging the gap on the relative roles of hydraulic, diffusive and biochemical constraints to photosynthesis. PLoS ONE 9:e95571. https://doi.org/10.1371/journal.pone.0095571
Martins SCV, Sanglard ML, Morais LE, Menezes-Silva PE, Mauri R, Avila RT, Vital CE, Cardoso AA, DaMatta FM (2019) How do coffee trees deal with severe natural droughts? An analysis of hydraulic, diffusive and biochemical components at the leaf leve. Trees. https://doi.org/10.1007/s00468-019-01889-4
Melo EF, Fernandes-Brum CN, Pereira FJ, Castro EM, Chalfun-Júnior A (2014) Anatomic and physiological modifications in seedlings of Coffea arabica cultivar Siriema under drought conditions. Ciênc Agrotec 38:25–33. https://doi.org/10.1590/S1413-70542014000100003
Nishiyama Y, Allakhverdiev SI, Murata N (2011) Protein synthesis is the primary target of reactive oxygen species in the photoinhibition of photosystem II. Physiol Plant 142:35–46. https://doi.org/10.1111/j.1399-3054.2011.01457.x
Ogle DH, Wheeler P, Dinno A (2020) FSA: fisheries stock analysis. R package version 0.8.31. https://github.com/droglenc/FSA. Accessed 25 January 2021
Paknejad F, Nasri M, Moghadam HRT, Zahedi H, Alahmadi MJ (2007) Effects of drought stress on chlorophyll fluorescence parameters, chlorophyll content and grain yield of wheat cultivars. J Biol Sci 7:841–847. https://doi.org/10.3923/jbs.2007.841.847
Parry MAJ, Andralojc J, Khan S, Lea PJ, Keys AJ (2002) Rubisco activity: effects of drought stress. Ann Bot 89:833–839. https://doi.org/10.1093/aob/mcf103
Pereira FJ, Castro EM, Souza TC, Magalhães PC (2008) Evolução da anatomia radicular do milho ‘Saracura’ em ciclos de seleção sucessivos. Pesqui Agropecu Bras 43:1649–1656. https://doi.org/10.1590/S0100-204X2008001200002
Pitman WD, Holt EC, Conrad BE, Bashaw EC (1983) Histological differences in mointure-stressed and nonstressed kleingrass forage. Crop Sci 23:793–795. https://doi.org/10.2135/cropsci1983.0011183X002300040046x
Pohlert T (2020) PMCMRplus: calculate pairwise multiple comparisons of mean rank sums extended. R package version 1.7.1. https://CRAN.R-project.org/package=PMCMRplus. Accessed 25 January 2021
Prince SJ, Murphy M, Mutava RN, Durnell LA, Valliyodan B, Shannon JG, Nguyen HT (2017) Root xylem plasticity to improve water use and yield in water-stressed soybean. J Exp Bot 68:2027–2036. https://doi.org/10.1093/jxb/erw472
Rakocevic M, Matsunaga FT (2018) Variations in leaf growth parameters within the tree structure of adult Coffea arabica in relation to seasonal growth, water availability and air carbon dioxide concentration. Ann Bot 122:117–131. https://doi.org/10.1093/aob/mcy042
Ramachandran P, Wang G, Augstein F, De Vries J, Carlsbecker A (2018) Continuous root xylem formation and vascular acclimation to water deficit involves endodermal ABA signalling via miR165. Development. https://doi.org/10.1242/dev.159202
Reis AM (2014) Caracterização morfofisiológica de genótipos de Coffea arabica sob deficit hídrico. 51f. Dissertação (Mestrado em Agronomia/Fitotecnia)—Universidade Federal de Lavras, Lavras, MG.
Royston P (1995) Remark AS R94: a remark on algorithm AS 181: the W test for normality. J R Stat Soc Ser C (appl Stat) 44:547–551. https://doi.org/10.2307/2986146
Seo DH, Seomun S, Choi YD, Jang G (2020) Root development and stress tolerance in rice: the key to improving stress tolerance without yield penalties. Int J Mol Sci 21:1807. https://doi.org/10.3390/ijms21051807
Sharkey TD (2016) What gas exchange data can tell us about photosynthesis. Plant Cell Environ 39:1161–1163. https://doi.org/10.1111/pce.12641
Silva L, Marchiori PER, Maciel CP, Machado EC, Ribeiro RV (2010) Fotossíntese, relações hídricas e crescimento de cafeeiros jovens em relação à disponibilidade de fósforo. Pesqui Agropecu Bras 45:965–972. https://doi.org/10.1590/S0100-204X2010000900005
Silva VA, Abrahao JCR, Carvalho GR, Botelho CE, Volpato MML, Oliveira ACB, Pereira AA (2019) Conheça as novas cultivares de café tolerantes à seca. Revista Cultivar Grandes Culturas 247:6–8
Thalmann M, Santelia D (2017) Starch as a determinant of plant fitness under abiotic stress. New Phytol 214:943–951. https://doi.org/10.1111/nph.14491
Wintgens JN (2004) The coffee plant. In: Wintgens JN (ed) Coffee: growing, processing, sustainable production: a guidebook for growers, processors, traders, and researchers, Chapter 1. Wiley, New York, pp 1–24. https://doi.org/10.1002/9783527619627.ch1
Yuste J, Gutierrez I, Rubio JA, Alburquerque MV (2004) Réponse des potentiels hydriques de la feuille et du xylème comme indicateurs de l’état hydrique de la vigne, cépage tempranillo, soumis à différents régimes hydriques dans la vallée du douro. J Int Sci Vigne Vin 38:21–26
Zarebanadkouki M, Trtik P, Hayat F, Carminati A, Kaestner A (2019) Root water uptake and its pathways across the root: quantification at the cellular scale. Sci Rep 9:12979. https://doi.org/10.1038/s41598-019-49528-9
Acknowledgements
The authors acknowledge Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES/BR—Finance Code 001); Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq); Fundação de Amparo à Pesquisa do Estado de Minas Gerais (FAPEMIG). The authors also thank the Instituto Nacional de Ciência e Tecnologia do Café (INCT-Café) and the Consórcio Brasileiro de Pesquisa e Desenvolvimento do Café – Consórcio Pesquisa Café for the financial support and scholarships granted. PERM acknowledges the CNPq via grant #312663/2021-8.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by E. Kuzniak-Gebarowska.
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.
Rights and permissions
Springer Nature or its licensor 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
de Andrade, L.I.F., Linhares, P.C.A., da Fonseca, T.M. et al. Photosynthetic efficiency and root plasticity promote drought tolerance in coffee genotypes. Acta Physiol Plant 44, 109 (2022). https://doi.org/10.1007/s11738-022-03434-2
Received:
Revised:
Accepted:
Published:
DOI: https://doi.org/10.1007/s11738-022-03434-2