Abstract
Drought is the most prominent limiting factor to crop productivity. Banana, one of the most important food crops globally, is highly susceptible to drought. However, how banana plants respond to drought stress and post-drought recovery remains unclear. Therefore, this study determined the morphological and protein responses of banana plants (Musa acuminata cultivar Berangan) affected by drought stress, followed by recovery. The results showed that drought significantly reduced the leaf area, plant height, fresh weight, stem circumference, leaf relative water content, chlorophyll contents, and root length of the bananas. In contrast, relative electrolyte leakage, proline, malondialdehyde (MDA) and hydrogen peroxide contents, and the activities of antioxidant enzymes, including catalase (CAT), ascorbate peroxidase (APX), glutathione reductase (GR), peroxidase, and superoxide dismutase, were induced in the drought-treated banana leaves. However, after recovering from drought stress, the relative water content, MDA, hydrogen peroxide, and antioxidant enzyme activities, including CAT, APX, and GR, were comparable with well-watered plants. To determine the protein responses of bananas toward drought stress, the well-watered, drought-stressed, and recovered banana leaves were sampled for tandem mass tags-based quantitative proteomics analysis. Of the 1018 differentially abundant proteins, 274 were significantly changed. The identified proteins differing between the treatments were mainly related to carbohydrate, energy and amino acid metabolisms, genetic information processing, and secondary metabolite biosynthesis. Our data may assist in developing a complete proteome dataset which could be valuable for developing drought-tolerant bananas.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data Availability
The datasets generated during and/or analysed during the current study are available in the ProteomeXchange consortium via the PRoteomics IDEntifications (PRIDE, http://www.ebi.ac.uk/pride), with the dataset identifier PXD038335.
References
Aebi H (1984) Catalase in vitro. Methods Enzymol 105:121–126. https://doi.org/10.1016/S0076-6879(84)05016-3
Aghaie P, Tafreshi SAH (2020) Central role of 70-kDa heat shock protein in adaptation of plants to drought stress. Cell Stress Chaperones 25:1071–1081. https://doi.org/10.1007/s12192-020-01144-7
Alagesan A, Padmanaban B, Tharani G, Jawahar S, Manivannan S (2019) An assessment of biological control of the banana pseudostem weevil Odoiporus longicollis (Olivier) by entomopathogenic fungi Beauveria bassiana. Biocatal Agric Biotechnol 20:101262. https://doi.org/10.1016/j.bcab.2019.101262
Amnan MAM, Aizat WM, Khaidizar FD, Tan BC (2022) Drought stress induces morpho-physiological and proteome changes of Pandanus amaryllifolius. Plants 11:1–21. https://doi.org/10.3390/plants11020221
Arellano JB (2023) Non-photochemical quenching of photosystem I as an adaptive response to prolonged drought. J Exp Bot 74:16–18. https://doi.org/10.1093/jxb/erac438
Bailey-Serres J, Voesenek LACJ (2008) Flooding stress: acclimations and genetic diversity. Annu Rev Plant Biol 59:313–339. https://doi.org/10.1146/annurev.arplant.59.032607.092752
Basu PS, Chaturvedi SK, Gaur PM, Mondal B, Meena SK, Das K, Kumar V, Tewari K, Sharma K (2022) Physiological mechanisms of tolerance to drought and heat in major pulses for improving yield under stress environments. In: Kimatu PJN (ed) Advances in plant defense mechanisms. IntechOpen, Rijeka, pp 314–346. https://doi.org/10.5772/intechopen.106054
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
Biswal AK, Pattanayak GK, Pandey SS, Leelavathi S, Reddy VS, Govindjee, Tripathy BC (2012) Light intensity-dependent modulation of chlorophyll b biosynthesis and photosynthesis by overexpression of chlorophyllide a oxygenase in tobacco. Plant Physiol 159:433–449. https://doi.org/10.1104/pp.112.195859
Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254. https://doi.org/10.1016/0003-2697(76)90527-3
Budzinski IGF, de Moraes FE, Cataldi TR, Franceschini LM, Labate CA (2019) Network analyses and data integration of proteomics and metabolomics from leaves of two contrasting varieties of sugarcane in response to drought. Front Plant Sci 10:1–19. https://doi.org/10.3389/fpls.2019.01524
Cantalapiedra CP, Hernandez-Plaza A, Letunic I, Bork P, Huerta-Cepas J (2021) eggNOG-mapper v2: functional annotation, orthology assignments, and domain prediction at the metagenomic scale. Mol Biol Evol 38:5825–5829. https://doi.org/10.1093/molbev/msab293
Carlberg I, Mannervik B (1975) Purification and characterization of the flavoenzyme glutathione reductase from rat liver. J Biol Chem 250:5475–5480
Carpentier SC, Witters E, Laukens K, Van Onckelen H, Swennen R, Panis B (2007) Banana (Musa spp.) as a model to study the meristem proteome: acclimation to osmotic stress. Proteomics 7(1):92–105. https://doi.org/10.1002/pmic.200600533
Çevik S, Akpinar G, Yildizli A, Kasap M, Karaosmanoğlu K, Ünyayar S (2019) Comparative physiological and leaf proteome analysis between drought-tolerant chickpea Cicer reticulatum and drought-sensitive chickpea C. arietinum. J Biosci 44:1–13. https://doi.org/10.1007/s12038-018-9836-4
Chin WYW, Annuar MSM, Tan BC, Khalid N (2014) Evaluation of a laboratory scale conventional shake flask and a bioreactor on cell growth and regeneration of banana cell suspension cultures. Sci Hortic 172:39–46. https://doi.org/10.1016/j.scienta.2014.03.042
Correia B, Hancock RD, Amaral J, Gomez-Cadenas A, Valledor L, Pinto G (2018) Combined drought and heat activates protective responses in Eucalyptus globulus that are not activated when subjected to drought or heat stress alone. Front Plant Sci 9:1–14. https://doi.org/10.3389/fpls.2018.00819
Dalal VK, Tripathy BC (2012) Modulation of chlorophyll biosynthesis by water stress in rice seedlings during chloroplast biogenesis. Plant Cell Environ 35:1685–1703. https://doi.org/10.1111/j.1365-3040.2012.02520.x
Davoudi M, Chen J, Lou Q (2022) Genome-wide identification and expression analysis of heat shock protein 70 (HSP70) gene family in pumpkin (Cucurbita moschata) rootstock under drought stress suggested the potential role of these chaperones in stress tolerance. Int J Mol Sci 23:1–16. https://doi.org/10.3390/ijms23031918
Dhindsa RS, Plumb-dhindsa P, Thorpe TA (1981) Leaf senescence: correlated with increased levels of membrane permeability and lipid peroxidation, and decreased levels of superoxide dismutase and catalase. J Exp Bot 32:93–101
Dikšaitytė A, Viršilė A, Žaltauskaitė J, Januškaitienė I, Juozapaitienė G (2019) Growth and photosynthetic responses in Brassica napus differ during stress and recovery periods when exposed to combined heat, drought and elevated CO2. Plant Physiol Biochem 142:59–72. https://doi.org/10.1016/j.plaphy.2019.06.026
Diniz AL, da Silva DIR, Lembke CG, Costa MDBL, Ten-Caten F, Li F, Vilela RD, Menossi M, Ware D, Endres L, Souza GM (2020) Amino acid and carbohydrate metabolism are coordinated to maintain energetic balance during drought in sugarcane. Int J Mol Sci 21:1–27. https://doi.org/10.3390/ijms21239124
Du CX, Fan HF, Guo SR, Tezuka T, Li J (2010) Proteomic analysis of cucumber seedling roots subjected to salt stress. Phytochemistry 71:1450–1459. https://doi.org/10.1016/j.phytochem.2010.05.020
Eid MAM, El-hady MAA, Abdelkader MA, Abd-Elkrem YM, El-Gabry YA, El-temsah ME, El-Areed SRM, Rady MM, Alamer KH, Alqubaie AI, Ali EF (2022) Response in physiological traits and antioxidant capacity of two cotton cultivars under water limitations. Agronomy 12:803. https://doi.org/10.3390/agronomy12040803
El-Mahdy MT, Abdel-Wahab DA, Youssef M (2021) In vitro morpho-physiological performance and DNA stability of banana under cadmium and drought stresses. In Vitro Cell Dev Biol-Plant 57:460–469. https://doi.org/10.1007/s11627-020-10142-4
ElSayed AI, El-hamahmy MAM, Rafudeen MS, Mohamed AH, Omar AA (2019) The impact of drought stress on antioxidant responses and accumulation of flavonolignans in milk thistle (Silybum marianum (L.) Gaertn). Plants 8:611. https://doi.org/10.3390/plants8120611
Fadoul HE, El Siddig MA, Abdalla AWH, El Hussein AA (2018) Physiological and proteomic analysis of two contrasting Sorghum bicolor genotypes in response to drought stress. Aust J Crop Sci 12:1543–1551. https://doi.org/10.21475/ajcs.18.12.09.PNE134
Gharechahi J, Hajirezaei MR, Salekdeh GH (2015) Comparative proteomic analysis of tobacco expressing cyanobacterial flavodoxin and its wild type under drought stress. J Plant Physiol 175:48–58. https://doi.org/10.1016/j.jplph.2014.11.001
Hasanuzzaman M, Bhuyan MHMB, Zulfiqar F, Raza A, Mohsin SM, Al Mahmud J, Fujita M, Fotopoulos V (2020) Reactive oxygen species and antioxidant defense in plants under abiotic stress: revisiting the crucial role of a universal defense regulator. Antioxidants 9(8):1–52. https://doi.org/10.3390/antiox9080681
Heath RL, Packer L (1968) Photoperoxidation in isolated chloroplasts. Arch Biochem Biophys 125:189–198. https://doi.org/10.1016/0003-9861(68)90654-1
Hu W, Ding Z, Tie W et al (2017) Comparative physiological and transcriptomic analyses provide integrated insight into osmotic, cold, and salt stress tolerance mechanisms in banana. Sci Rep 7:1–12. https://doi.org/10.1038/srep43007
Huang B, Xu Y (2015) Cellular and molecular mechanisms for elevated CO2—Regulation of plant growth and stress adaptation. Crop Sci 55:1405–1424. https://doi.org/10.2135/cropsci2014.07.0508
Huerta-Cepas J, Szklarczyk D, Heller D, Hernández-Plaza A, Forslund SK, Cook H, Mende DR, Letunic I, Rattei T, Jensen LJ, Von Mering C, Bork P (2019) EggNOG 5.0: a hierarchical, functionally and phylogenetically annotated orthology resource based on 5090 organisms and 2502 viruses. Nucleic Acids Res 47:D309–D314. https://doi.org/10.1093/nar/gky1085
Jacques B, Coinçon M, Sygusch J (2018) Active site remodeling during the catalytic cycle in metal-dependent fructose-1,6-bisphosphate aldolases. J Biol Chem 293:7737–7753. https://doi.org/10.1074/jbc.RA117.001098
Jan N, Rather AMUD, John R, Chaturvedi P, Ghatak A, Weckwerth W, Zargar SM, Mir RA, Khan MA, Mir RR (2022) Proteomics for abiotic stresses in legumes: present status and future directions. Crit Rev Biotechnol 0:1–20. https://doi.org/10.1080/07388551.2021.2025033
Kerner R, Delgado-Eckert E, Del Castillo E, Müller-Starck G, Peter M, Kuster B, Tisserant E, Pritsch K (2012) Comprehensive proteome analysis in Cenococcum geophilum Fr. As a tool to discover drought-related proteins. J Proteom 75:3707–3719. https://doi.org/10.1016/j.jprot.2012.04.039
Khueychai S, Jangpromma N, Daduang S, Jaisil P, Lomthaisong K, Dhiravisit A, Klaynongsruang S (2015) Comparative proteomic analysis of leaves, leaf sheaths, and roots of drought-contrasting sugarcane cultivars in response to drought stress. Acta Physiol Plant 37:88. https://doi.org/10.1007/s11738-015-1826-7
Kim SG, Lee JS, Kim JT, Kwon YS, Bae DW, Bae HH, Son BY, Baek SB, Kwon YU, Woo MO, Shin S (2015) Physiological and proteomic analysis of the response to drought stress in an inbred korean maize line. Plant Omics 8:159–168
Lau S-E, Hamdan MF, Pua T-L, Saidi NB, Tan BC (2021) Plant nitric oxide signaling under drought stress. Plants 10:360. https://doi.org/10.3390/plants10020360
Lau SE, Teo WFA, Teoh EY, Tan BC (2022) Microbiome engineering and plant biostimulants for sustainable crop improvement and mitigation of biotic and abiotic stresses. Discov Food 2:1–23. https://doi.org/10.1007/s44187-022-00009-5
Li H, Yang M, Zhao C, Wang Y, Zhang R (2021) Physiological and proteomic analyses revealed the response mechanisms of two different drought-resistant maize varieties. BMC Plant Biol 21:1–15. https://doi.org/10.1186/s12870-021-03295-w
Lichtenthaler HK, Buschmann C (2001) Chlorophylls and carotenoids: measurement and characterization by UV-VIS spectroscopy. Curr Protoc Food Anal Chem 1:F4.3.1-F4.3.8
Lv Y, Li Y, Liu X, Xu K (2020) Photochemistry and proteomics of ginger (Zingiber officinale Roscoe) under drought and shading. Plant Physiol Biochem 151:188–196. https://doi.org/10.1016/j.plaphy.2020.03.021
Mahouachi J (2009) Changes in nutrient concentrations and leaf gas exchange parameters in banana plantlets under gradual soil moisture depletion. Sci Hortic 120:460–466. https://doi.org/10.1016/j.scienta.2008.12.002
Mattos-Moreira LA, Ferreira CF, Amorim EP, Pirovani CP, de Andrade EM, Filho MAC, da Silva Ledo CA (2018) Differentially expressed proteins associated with drought tolerance in bananas (Musa spp.). Acta Physiol Plant 40:60. https://doi.org/10.1007/s11738-018-2638-3
Merlaen B, De Keyser E, Ding L, Leroux O, Chaumont F, Van Labeke MC (2019) Physiological responses and aquaporin expression upon drought and osmotic stress in a conservative vs prodigal Fragaria × ananassa cultivar. Plant Physiol Biochem 145:95–106. https://doi.org/10.1016/j.plaphy.2019.10.030
Mohd Amnan MA, Pua T-L, Lau S-E, Tan BC, Yamaguchi H, Hitachi K, Tsuchida K, Komatsu S (2021) Osmotic stress in banana is relieved by exogenous nitric oxide. PeerJ 9:e10879. https://doi.org/10.7717/peerj.10879
Mohd Amnan MA, Teo WFA, Aizat WM, Khaidizar FD, Tan BC (2023) Foliar application of oil palm wood vinegar enhances Pandanus amaryllifolius tolerance under drought stress. Plants 12:785. https://doi.org/10.3390/plants12040785
Moloi MJ, Van Merwe R (2021) Drought tolerance responses in vegetable-type soybean and pod-filling stages. Plants 10:1502. https://doi.org/10.3390/plants10081502
Muthusamy M, Uma S, Backiyarani S, Saraswathi MS, Chandrasekar A (2016) Transcriptomic changes of drought-tolerant and sensitive banana cultivars exposed to drought stress. Front Plant Sci 7:1609. https://doi.org/10.3389/fpls.2016.01609
Nakano Y, Asada K (1981) Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplasts. Plant Cell Physiol 22(5):867–880. https://doi.org/10.1093/oxfordjournals.pcp.a076232
Oh MW, Komatsu S (2015) Characterization of proteins in soybean roots under flooding and drought stresses. J Proteom 114:161–181. https://doi.org/10.1016/j.jprot.2014.11.008
Pan J, Li Z, Wang Q, Garrell AK, Liu M, Guan Y, Zhou W, Liu W (2018) Comparative proteomic investigation of drought responses in foxtail millet. BMC Plant Biol 18:1–19. https://doi.org/10.1186/s12870-018-1533-9
Piveta LB, Roma-Burgos N, Noldin JA, Viana VE, de Oliveira C, Lamego FP, de Avila LA (2021) Molecular and physiological responses of rice and weedy rice to heat and drought stress. Agriculture 11:1–23. https://doi.org/10.3390/agriculture11010009
Pourghayoumi M, Rahemi M, Bakhshi D et al (2017) Responses of pomegranate cultivars to severe water stress and recovery: changes on antioxidant enzyme activities, gene expression patterns and water stress responsive metabolites. Physiol Mol Biol Plants 23:321–330. https://doi.org/10.1007/s12298-017-0435-x
Pütter J (1974) Peroxidases. Methods Enzym Anal 685:690. https://doi.org/10.1016/b978-0-12-091302-2.50033-5
Quan W, Hu Y, Mu Z, Shi H, Chan Z (2018) Overexpression of AtPYL5 under the control of guard cell specific promoter improves drought stress tolerance in Arabidopsis. Plant Physiol Biochem 129:150–157. https://doi.org/10.1016/j.plaphy.2018.05.033
Ramakrishna G, Singh A, Kaur P, Yadav SS, Sharma S, Gaikwad K (2022) Genome wide identification and characterization of small heat shock protein gene family in pigeonpea and their expression profiling during abiotic stress conditions. Int J Biol Macromol 197:88–102. https://doi.org/10.1016/j.ijbiomac.2021.12.016
Rhythm, Sharma P, Sardana V, Czern L (2022) Physiological and biochemical traits of drought tolerance in Brassica juncea Czern & Coss South African J Bot 146:509–520. https://doi.org/10.1016/j.sajb.2021.11.019
Sun W, Bernard C, Van Cotte B, Van De M, Verbruggen N (2001) At-HSP17.6A, encoding a small heat-shock protein in Arabidopsis, can enhance osmotolerance upon overexpression. Plant J 27:407–415. https://doi.org/10.1046/j.1365-313X.2001.01107.x
Sun W, Shahrajabian MH, Cheng Q (2021) The roles of a light-dependent protochlorophyllide oxidoreductase (LPOR), and ATP-dependent dark operative protochlorophyllide oxidoreductase (DPOR) in chlorophyll biosynthesis. Not Bot Horti Agrobot Cluj-Napoca 49:1–15. https://doi.org/10.15835/nbha49312456
Svensk M, Coste S, Gérard B, Gril E, Julien F, Maillard P, Stahl C, Leroy C (2020) Drought effects on resource partition and conservation among leaf ontogenetic stages in epiphytic tank bromeliads. Physiol Plant 170(4):488–507. https://doi.org/10.1111/ppl.13161
Szabados L, Savouré A (2010) Proline: a multifunctional amino acid. Trends Plant Sci 15:89–97. https://doi.org/10.1016/j.tplants.2009.11.009
Tak H, Negi S, Ganapathi TR (2017) Banana NAC transcription factor MusaNAC042 is positively associated with drought and salinity tolerance. Protoplasma 254:803–816. https://doi.org/10.1007/s00709-016-0991-x
Talla SK, Bagari P, Manga S, Aileni M, Mamidala P (2022) Comparative study of micropropagated plants of Grand Naine banana during in vitro regeneration and ex vitro acclimatization. Biocatal Agric Biotechnol 42:102325. https://doi.org/10.1016/j.bcab.2022.102325
Tan BC (2022) Can banana be a success story for Malaysia? J Agribus Mark 9:13–22. https://doi.org/10.56527/jabm.9.1.2
Tan BC, Lim YS, Lau SE (2017) Proteomics in commercial crops: an overview. J Proteom 169:176–188. https://doi.org/10.1016/j.jprot.2017.05.018
Thimm O, Bläsing O, Gibon Y, Nagel A, Meyer S, Krüger P, Selbig J, Müller LA, Rhee SY, Stitt M (2004) MAPMAN: a user-driven tool to display genomics data sets onto diagrams of metabolic pathways and other biological processes. Plant J 37:914–939. https://doi.org/10.1111/j.1365-313X.2004.02016.x
Vanhove A-C, Vermaelen W, Panis B, Swennen R, Carpentier SC (2012) Screening the banana biodiversity for drought tolerance: can an in vitro growth model and proteomics be used as a tool to discover tolerant varieties and understand homeostasis. Front Plant Sci 3:176. https://doi.org/10.3389/fpls.2012.00176
Vantyghem M, Merckx R, Stevens B, Hood-Nowotny R, Swennen R, Dercon G (2022) The potential of stable carbon isotope ratios and leaf temperature as proxies for drought stress in banana under field conditions. Agric Water Manag 260:107247. https://doi.org/10.1016/j.agwat.2021.107247
Varma V, Bebber DP (2019) Climate change impacts on banana yields around the world. Nat Clim Chang 9:752–757. https://doi.org/10.1038/s41558-019-0559-9
Velikova V, Yordanov I, Edreva A (2000) Oxidative stress and some antioxidant systems in acid rain-treated bean plants: protective role of exogenous polyamines. Plant Sci 151:59–66. https://doi.org/10.1016/S0168-9452(99)00197-1
Verslues PE, Bailey-Serres J, Brodersen C, Buckley TN, Conti L, Christmann A, Dinneny JR, Grill E, Hayes S, Heckman RW, Hsu PK, Juenger TE, Mas P, Munnik T, Nelissen H, Sack L, Schroeder JI, Testerink C, Tyerman SD et al (2023) Burning questions for a warming and changing world: 15 unknowns in plant abiotic stress. Plant Cell 35(1):67–108. https://doi.org/10.1093/plcell/koac263
Wang Y, Xu C, Zhang B, Wu M, Chen G (2017) Physiological and proteomic analysis of rice (Oryza sativa L.) in flag leaf during flowering stage and milk stage under drought stress. Plant Growth Regul 82:201–218. https://doi.org/10.1007/s10725-017-0252-9
Wang N, Liu W, Yu L, Guo Z, Chen Z, Jiang S et al (2020) HEAT SHOCK FACTOR A8a modulates flavonoid synthesis and drought tolerance. Plant Physiol 184(3):1273–1290. https://doi.org/10.1104/pp.20.01106
Wang A, Ma C, Ma H, Qiu Z, Wen X (2021) Physiological and proteomic responses of pitaya to PEG-induced drought stress. Agriculture 11:632. https://doi.org/10.3390/agriculture11070632
Wang X, Li Y, Wang X, Li X, Dong S (2022) Physiology and metabonomics reveal differences in drought resistance among soybean varieties. Bot Stud 63:1–15. https://doi.org/10.1186/s40529-022-00339-8
Wu J, Gao T, Hu J, Zhao L, Yu C, Ma F (2022) Research advances in function and regulation mechanisms of plant small heat shock proteins (sHSPs) under environmental stresses. Sci Total Environ 825:154054. https://doi.org/10.1016/j.scitotenv.2022.154054
Xiao S, Liu L, Zhang Y, Sun H, Zhang K, Bai Z, Dong H, Liu Y, Li C (2020) Tandem mass tag-based (TMT) quantitative proteomics analysis reveals the response of fine roots to drought stress in cotton (Gossypium hirsutum L). BMC Plant Biol 20:328. https://doi.org/10.1186/s12870-020-02531-z
Xu YH, Liu R, Yan L, Liu ZQ, Jiang SC, Shen YY, Wang XF, Zhang DP (2012) Light-harvesting chlorophyll a/b-binding proteins are required for stomatal response to abscisic acid in Arabidopsis. J Exp Bot 63:1095–1106. https://doi.org/10.1093/jxb/err315
Xu B, Gao X, Dong K, Li X, Yang P, Yang T, Feng B (2020) Grain protein content comparison and proteomic analysis of foxtail millet (Setaria italica L.) seed response to different drought stress levels. Acta Physiol Plant 42:1–11. https://doi.org/10.1007/s11738-019-2999-2
Yahoueian SH, Bihamta MR, Babaei HR, Bazargani MM (2021) Proteomic analysis of drought stress response mechanism in soybean (Glycine max L.) leaves. Food Sci Nutr 9:2010–2020. https://doi.org/10.1002/fsn3.2168
Yan M, Zheng L, Li B, Shen R, Lan P (2021) Comparative proteomics reveals new insights into the endosperm responses to drought, salinity and submergence in germinating wheat seeds. Plant Mol Biol 105:287–302. https://doi.org/10.1007/s11103-020-01087-8
Ye T, Shi H, Wang Y, Chan Z (2015) Contrasting changes caused by drought and submergence stresses in bermudagrass (Cynodon dactylon). Front Plant Sci 6:951. https://doi.org/10.3389/fpls.2015.00951
Yu MH, Ding GD, Gao GL, Zhao YY, Yan L, Sai K (2015) Using plant temperature to evaluate the response of stomatal conductance to soil moisture deficit. Forests 6:3748–3762. https://doi.org/10.3390/f6103748
Zadražnik T, Egge-Jacobsen W, Meglič V, Šuštar-Vozlič J (2017) Proteomic analysis of common bean stem under drought stress using in-gel stable isotope labeling. J Plant Physiol 209:42–50. https://doi.org/10.1016/j.jplph.2016.10.015
Zargar SM, Gupta N, Nazir M, Mahajan R, Malik FA, Sofi NR, Shikari AB, Salgotra RK (2017) Impact of drought on photosynthesis: molecular perspective. Plant Gene 11:154–159. https://doi.org/10.1016/j.plgene.2017.04.003
Zhang J, Chen H, Wang H, Li B, Yi Y, Kong F, Liu J, Zhang H (2016) Constitutive expression of a tomato small heat shock protein gene LeHSP21 improves tolerance to high-temperature stress by enhancing antioxidation capacity in tobacco. Plant Mol Biol Report 34:399–409. https://doi.org/10.1007/s11105-015-0925-3
Zhang D, Yang Z, Song X, Zhang F, Liu Y (2022) TMT-based proteomic analysis of liquorice root in response to drought stress. BMC Genomics 23:1–17. https://doi.org/10.1186/s12864-022-08733-z
Zhou Y, Lam HM, Zhang J (2007) Inhibition of photosynthesis and energy dissipation induced by water and high light stresses in rice. J Exp Bot 58:1207–1217. https://doi.org/10.1093/jxb/erl291
Zhou J, Reddy S, Zhou S, Sauvé RJ, Bhatti S, Fish T, Thannhauser TW (2012) Effect of heat stress on leaf proteome and enzyme activity in Solanum chilense. Plant Stress 6:8–13
Zhu D, Luo F, Zou R et al (2021) Integrated physiological and chloroplast proteome analysis of wheat seedling leaves under salt and osmotic stresses. J Proteom 234:104097. https://doi.org/10.1016/j.jprot.2020.104097
Acknowledgements
The first author thanked Muhammad Asyraf Mohd Amnan for his technical assistance. This research was supported by the Ministry of Higher Education Malaysia under the Fundamental Research Grant Scheme (FRGS/1/2018/STG03/UM/02/2), Royal Society-Newton Advanced Fellowship (IF004-2018), and the Southeast Asian University Consortium for Graduate Education in Agriculture and Natural Resources under the University Consortium Student Thesis Grant for Research Activities (GBG22-0919).
Author information
Authors and Affiliations
Contributions
Conceptualization: BCT, TLP, NBS, JOA and DUL. Methodology and data analysis: SEL, BCT and TLP. Writing—original draft preparation: SEL and BCT. Writing—review and editing: BCT, TLP, NBS, JOA and DUL. Supervision: BCT, NBS, JOA and DUL. Funding acquisition: BCT. All authors have read and agreed to the published version of the manuscript.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare the absence of conflict of interest.
Additional information
Handling Editor: Christian Chervin.
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 (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
Lau, SE., Pua, TL., Saidi, N.B. et al. Combined Proteomics and Physiological Analyses Reveal Drought and Recovery Response Mechanisms in Banana Leaves. J Plant Growth Regul 42, 7624–7648 (2023). https://doi.org/10.1007/s00344-023-11039-3
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00344-023-11039-3