Abstract
Main conclusion
Inbred line 11–133 of popcorn showed the lowest apoplast Al and total Al concentrations and Al-lumogallion complex, associated with a more efficient antioxidant system, mainly due to glutathione metabolism.
Abstract
Popcorn (Zea mays L. var. everta) is largely intended for human consumption. About 40% of the world’s arable soils are acidic. In soils acidic, aluminum (Al) ionizes producing the trivalent cation, which is highly toxic to plants. Hence, this work aimed to: (1) evaluate the Al toxicity sites and its effect on the structure of the root tips, (2) quantify Al concentrations in the apoplast and symplast of the roots, and (3) to elucidate the modulation on the activity of antioxidant enzymes and metabolites of the ascorbate–glutathione cycle in two popcorn inbred lines (ILs) 11–133 and 11–60, classified as tolerant and sensitive to this metal, respectively. Aluminum toxicity did not affect the shoot growth; however, there was a yellowing of the oldest leaf blade only in 11–60. The better performance of 11–133 is related to lower apoplastic and total Al concentrations and Al accumulation in the root associated with a lower fluorescence of Al–lumogallion complex at the root tip, indicating the presence of mechanisms of chelation with this metal. Consequently, this IL showed less change in root morphoanatomy and lower reactive oxygen species and malondialdehyde content, which are associated with a more efficient enzymatic and non-enzymatic system, mainly due to the higher content of the glutathione metabolite and the higher activities of superoxide dismutase, monodehydroascorbate reductase, dehydroascorbate reductase, γ-glutamylcysteine synthetase, and glutathione peroxidase enzymes. Thus, these findings illustrated above indicate how internal mechanisms of detoxification respond to Al in popcorn, which can be used as tolerance biomarkers.
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Data availability
The datasets used and/or analyzed during the current study are available from the corresponding author on reasonable request.
Abbreviations
- AsA:
-
Ascorbate
- CAT:
-
Catalase
- DHAR:
-
Dehydroascorbate reductase
- DTZ:
-
Distal region of the transition zone
- GPX:
-
Glutathione peroxidase
- GSH:
-
Reduced glutathione
- GST:
-
Glutathione S-transferase
- ILs:
-
Inbred lines
- MDHAR:
-
Monodehydroascorbate reductase
- POX:
-
Total peroxidase
- ROS:
-
Reactive oxygen species
- SOD:
-
Superoxide dismutase
- γ-GCS:
-
γ-Glutamylcysteine synthetase
References
Anjum NA, Sharma P, Gill SS, Hasanuzzaman M, Khan EA, Kachhap K, Mohamed AA, Thangavel P, Devi GD, Vasudhevan P, Sofo A, Khan NA, Misra AN, Lukatkin AS, Singh HP, Pereira E, Tuteja N (2016) Catalase and ascorbate peroxidase—representative H2O2-detoxifying heme enzymes in plants. Environ Sci Pollut Res 23:19002–19029. https://doi.org/10.1007/s11356-016-7309-6
Awasthi JP, Saha B, Regon P, Sahoo S, Chowra U, Pradhan A, Roy A, Panda SK (2017) Morpho-physiological analysis of tolerance to aluminum toxicity in rice varieties of North East India. PLoS ONE 12:e0176357. https://doi.org/10.1371/journal.pone.0176357
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
Brito DS, Neri-Silva R, Ribeiro KVG, Peixoto PHP, Ribeiro C (2020) Effects of aluminum on the external morphology of root tips in rice. Braz J Bot 43:413–418. https://doi.org/10.1007/s40415-020-00620-9
Caniato FF, Guimarães CT, Schaffert RE, Alves VMC, Kochian LV, Borém A, Klein PE, Magalhaes JV (2007) Genetic diversity for aluminum tolerance in sorghum. Theor Appl Genet 114:863–876. https://doi.org/10.1007/s00122-006-0485-x
Chandra J, Keshavkant S (2021) Mechanisms underlying the phytotoxicity and genotoxicity of aluminum and their alleviation strategies: a review. Chemosphere 278:130–384. https://doi.org/10.1016/j.chemosphere.2021.130384
Chandra J, Parkhey S, Varghese D, Varghese B, Keshavkant S (2020) Aluminum rhizotoxicity in Cicer arietinum. Russ J Plant Physiol 67:945–952. https://doi.org/10.1134/S1021443720050027
Chowra U, Yanase E, Koyama H, Panda SK (2017) Aluminium-induced excessive ROS causes cellular damage and metabolic shifts in black gram Vigna mungo (L.) Hepper. Protoplasma 254:293–302. https://doi.org/10.1007/s00709-016-0943-5
Čiamporová M (2002) Morphological and structural responses of plant roots to aluminium at organ, tissue, and cellular levels. Biologia Plant 45:161–171. https://doi.org/10.1023/A:1015159601881
Clark RB (1975) Characterization of phosphatase of intact maize roots. J Agric Food Chem 23:458–460. https://doi.org/10.1021/jf60199a002
Foyer CH, Noctor G (2011) Ascorbate and glutathione: the heart of the redox hub. Plant Physiol 155:2–18. https://doi.org/10.1104/pp.110.167569
Furlan F, Borgo L, Rabêlo FHS, Rossi ML, Linhares FS, Martinelli AP, Azevedo RA, Lavres J (2020) Aluminum-induced toxicity in Urochloa brizantha genotypes: a first glance into root Al-apoplastic and -symplastic compartmentation, Al-translocation and antioxidant performance. Chemosphere 243:125362. https://doi.org/10.1016/j.chemosphere.2019.125362
García-Pinilla S, Gutiérrez-López GF, Hernández-Sánchez H, Cáez-Ramírez G, García-Armenta E, Alamilla-Beltrán L (2020) Quality parameters and morphometric characterization of hot-air popcorn as related to moisture content. Dry Technol 39:77–89. https://doi.org/10.1080/07373937.2019.1695626
Garzón T, Gunsé B, Moreno AR, Tomos AD, Barceló J, Poschenrieder C (2011) Aluminium-induced alteration of ion homeostasis in root tip vacuoles of two maize varieties differing in Al tolerance. Plant Sci 180:709–715. https://doi.org/10.1016/j.plantsci.2011.01.022
Gay C, Gebicki JM (2000) A critical evaluation of the effect of sorbitol on the ferric–xylenol orange hydroperoxide assay. Anal Biochem 284:217–220. https://doi.org/10.1006/abio.2000.4696
Giannakoula A, Moustakas M, Syros T, Yupsanis T (2010) Aluminum stress induces up-regulation of an efficient antioxidant system in the Al-tolerant maize line but not in the Al-sensitive line. Environ Exp Bot 67:487–494. https://doi.org/10.1016/j.envexpbot.2009.07.010
Giannopolitis CN, Ries SK (1977) Superoxide dismutases: I. occurrence in higher plants. Plant Physiol 59:309–314. https://doi.org/10.1104/pp.59.2.309
Guo P, Qi YP, Cai YT, Yang TY, Yang LT, Huang ZR, Chen LS (2018) Aluminum effects on photosynthesis, reactive oxygen species and methylglyoxal detoxification in two Citrus species differing in aluminum tolerance. Tree Physiol 38:1548–1565. https://doi.org/10.1093/treephys/tpy035
Habig WH, Jakoby WB (1981) [51] Assays for differentiation of glutathione S-transferases. Methods Enzymol 77:398–405. https://doi.org/10.1016/S0076-6879(81)77053-8
Havir EA, McHale NA (1987) Biochemical and developmental characterization of multiple forms of catalase in tobacco leaves. Plant Physiol 84:450–455. https://doi.org/10.1104/pp.84.2.450
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
Horst WJ, Wang Y, Eticha D (2010) The role of the root apoplast in aluminium-induced inhibition of root elongation and in aluminum resistance of plants: a review. Ann Bot 106:185–197. https://doi.org/10.1093/aob/mcq053
Kampfenkel K, Vanmontagu M, Inze D (1995) Extraction and determination of ascorbate and dehydroascorbate from plant tissue. Anal Biochem 225:165–167. https://doi.org/10.1006/abio.1995.1127
Kar M, Mishra D (1976) Catalase, peroxidase, and polyphenoloxidase activities during rice leaf senescence. Plant Physiol 57:315–319. https://doi.org/10.1104/pp.57.2.315
Kataoka T, Nakanishi TM (2001) Aluminum distribution in soybean root tip for a short time Al treatment. J Plant Physiol 158:731–736. https://doi.org/10.1078/0176-1617-00163
Kato Y, Miura E, Matsushima R, Sakamoto W (2007) White leaf sectors in yellow variegated2 are formed by viable cells with undifferentiated plastids. Plant Physiol 144:952–960. https://doi.org/10.1104/pp.107.099002
Kochian LV, Piñeros MA, Liu J, Magalhaes JV (2015) Plant adaptation to acid soils: the molecular basis for crop aluminum resistance. Annu Rev Plant Biol 66:571–598. https://doi.org/10.1146/annurev-arplant-043014-114822
Kollmeier M, Felle HH, Horst WJ (2000) Genotypical differences in aluminum resistance of maize are expressed in the distal part of the transition zone. Is reduced basipetal auxin flow involved in inhibition of root elongation by aluminum? Plant Physiol 122:945–956. https://doi.org/10.1104/pp.122.3.945
Lindeman W (1959) Observations on the behaviour of phosphate compounds in Chlorella at the transition from dark to light. Agricultural Univ, Wageningen
Lu H, Dong G, Hua H, Zhao W, Li J, Xu R (2020) Method for initially selecting Al-tolerant rice varieties based on the charge characteristics of their roots. Ecotoxicol Environ Saf 187:109813. https://doi.org/10.1016/j.ecoenv.2019.109813
Malta PG, Arcanjo-Silva S, Ribeiro C, Campos NV, Azevedo AA (2016) Rudgea viburnoides (Rubiaceae) overcomes the low soil fertility of the Brazilian Cerrado and hyperaccumulates aluminum in cell walls and chloroplasts. Plant Soil 408:369–384. https://doi.org/10.1007/s11104-016-2926-x
Maphumulo S, Derera J, Sibiya J, Mathew I (2021) Combining ability, gene action and heterosis analyses of maize lines that were developed for maize streak virus resistance and acidic soil tolerance. Euphytica 217:23. https://doi.org/10.1007/s10681-020-02754-z
Mohammadi M, Karr AL (2001) Superoxide anion generation in effective and ineffective soybean root nodules. J Plant Physiol 158:1023–1029. https://doi.org/10.1078/S0176-1617(04)70126-1
Murshed R, Lopez-Lauri F, Sallanon H (2008) Microplate quantification of enzymes of the plant ascorbate–glutathione cycle. Anal Biochem 383:320–322. https://doi.org/10.1016/j.ab.2008.07.020
Nagalakshmi N, Prasad MNV (2001) Responses of glutathione cycle enzymes and glutathione metabolism to copper stress in Scenedesmus bijugatus. Plant Sci 160:291–299. https://doi.org/10.1016/S0168-9452(00)00392-7
Nakano Y, Asada K (1981) Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplasts. Plant Cell Physiol 22:867–880. https://doi.org/10.1093/oxfordjournals.pcp.a076232
Nemat Alla MM, Badawi A-HM, Hassan NM, El-Bastawisy ZM, Badran EG (2008) Herbicide tolerance in maize is related to increased levels of glutathione and glutathione-associated enzymes. Acta Physiol Plant 30:371–379. https://doi.org/10.1007/s11738-008-0134-x
Noctor G, Strohm M, Jouanin L, Kunert KJ, Foyer CH, Rennenberg H (1996) Synthesis of glutathione in leaves of transgenic poplar overexpressing γ-glutamylcysteine synthetase. Plant Physiol 112:1071–1078. https://doi.org/10.1104/pp.112.3.1071
Paraginski RT, de Souza NL, Alves GH, Ziegler V, de Oliveira M, Elias MC (2016) Sensory and nutritional evaluation of popcorn kernels with yellow, white and red pericarps expanded in different ways. J Cereal Sci 69:383–391. https://doi.org/10.1016/j.jcs.2016.05.013
Pinto VB, Almeida VC, Pereira-Lima ÍA, Vale EM, Araújo WL, Silveira V, Viana JMS (2021a) Deciphering the major metabolic pathways associated with aluminum tolerance in popcorn roots using label-free quantitative proteomics. Planta 254:132. https://doi.org/10.1007/s00425-021-03786-y
Pinto VB, Ferreira PG, Vidigal PMP, Oliveira Mendes TA, Dal-Bianco M, de Magalhaes JV, Viana JMS (2021b) Uncovering the transcriptional response of popcorn (Zea mays L. var. everta) under long-term aluminum toxicity. Sci Rep 11:196–244. https://doi.org/10.1038/s41598-021-99097-z
Pirzadah TB, Malik B, Tahir I, Rehman RU, Hakeem KR, Alharby HF (2019) Aluminum stress modulates the osmolytes and enzyme defense system in Fagopyrum species. Plant Physiol Biochem 144:178–186. https://doi.org/10.1016/j.plaphy.2019.09.033
Polle E, Konzak CF, Kattrick JA (1978) Visual detection of aluminum tolerance levels in wheat by hematoxylin staining of seedling roots. Crop Sci 18:823–827. https://doi.org/10.2135/cropsci1978.0011183X001800050035x
R Core Team (2018) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. https://www.R-project.org/
Rahim F, Almeida VC, Viana JMS, Ribeiro C, Risso LA, Ribeiro MP (2019) Identification of contrasting tropical popcorn inbreds for studying aluminum toxicity tolerance inheritance. Euphytica 215:47. https://doi.org/10.1007/s10681-019-2372-y
Rahman I, Kode A, Biswas SK (2006) Assay for quantitative determination of glutathione and glutathione disulfide levels using enzymatic recycling method. Nat Protoc 1:3159–3165. https://doi.org/10.1038/nprot.2006.378
Ramakrishna B, Rao SSR (2013) Preliminary studies on the involvement of glutathione metabolism and redox status against zinc toxicity in radish seedlings by 28-homobrassinolide. Environ Exp Bot 96:52–58. https://doi.org/10.1016/j.envexpbot.2013.08.003
Ramírez-Benítez JE, Chee-González L, Teresa Hernandez-Sotomayor SM (2008) Aluminum induces changes in organic acids metabolism in Coffea arabica suspension cells with differential Al-tolerance. J Inorg Biochem 102:1631–1637. https://doi.org/10.1016/j.jinorgbio.2008.03.002
Ribeiro C, Cambraia J, Peixoto PHP, da Fonseca Júnior ÉM (2012) Antioxidant system response induced by aluminum in two rice cultivars. Braz J Plant Physiol 24:107–116. https://doi.org/10.1590/S1677-04202012000200004
Sarruge JR, Haag HP (1974) Análises químicas em plantas. Esalq, Piracicaba, p 56
Schmohl N, Pilling J, Fisahn J, Horst WJ (2000) Pectin methylesterase modulates aluminum sensitivity in Zea mays and Solanum tuberosum. Physiol Plant 109:419–427. https://doi.org/10.1034/j.1399-3054.2000.100408.x
Silva CO, Brito DS, da Silva AA, do Rosário RV, Santos MFS, de Souza GA, Azevedo AA, Dal-Bianco M, Oliveira JA, Ribeiro C (2020) Differential accumulation of aluminum in root tips of soybean seedlings. Braz J Bot 43:99–107. https://doi.org/10.1007/s40415-020-00593-9
Singh S, Tripathi DK, Singh S, Sharma S, Dubey NK, Chauhan DK, Vaculík M (2017) Toxicity of aluminumon various levels of plant cells and organism: a review. Environ Exp Bot 137:177–193. https://doi.org/10.1016/j.envexpbot.2017.01.005
Sivaguru M, Horst WJ (1998) The Distal part of the transition zone is the most aluminum-sensitive apical root zone of maize. Plant Physiol 116:155–163. https://doi.org/10.1104/pp.116.1.155
Sosa-Morales ME, Andaluz-Mejía LM, Cardona-Herrera R, Castañeda-Rodríguez LR, Ochoa-Montes DA, Santiesteban-López NA, Rojas-Laguna R (2022) Quality evaluation of yellow corn (Zea mays cv. Everta) subjected to 27.12-MHz radio frequency treatments for popcorn production. Int J Food Sci Tech 57:3263–3267. https://doi.org/10.1111/ijfs.15614
Sousa A, Saleh AM, Habeeb TH, Hassan YM, Zrieq R, Wadaan MAM, Hozzein WN, Selim S, Matos M, AbdElgawad H (2019) Silicon dioxide nanoparticles ameliorate the phytotoxic hazards of aluminum in maize grown on acidic soil. Sci Total Environ 693:133–636. https://doi.org/10.1016/j.scitotenv.2019.133636
Sun C, Liu L, Yu Y, Liu W, Lu L, Jin C, Lin X (2015) Nitric oxide alleviates aluminum-induced oxidative damage through regulating the ascorbate-glutathione cycle in roots of wheat: NO enhances wheat tolerance to Al toxicity. J Integr Plant Biol 57:550–561. https://doi.org/10.1111/jipb.12298
Taylor GJ, McDonald-Stephens JL, Hunter DB, Bertsch PM, Elmore D, Rengel Z, Reid RJ (2000) Direct measurement of aluminum uptake and distribution in single cells of Chara corallina. Plant Physiol 123:987–996. https://doi.org/10.1104/pp.123.3.987
Vittorazzi C, Júnior ATA, Guimarães AG, Viana AP, Silva FHL, Pena GF, Daher RF, Gerhardt IFS, Oliveira GHF, Pereira MG (2017) Research article indices estimated using REML/BLUP and introduction of a super-trait for the selection of progenies in popcorn. Genet Mol Res 16:1–10. https://doi.org/10.4238/gmr16039769
Wu D, Shen H, Yokawa K, Baluška F (2015) Overexpressing OsPIN2 enhances aluminuminternalization by elevating vesicular trafficking in rice root apex. J Exp Bot 66:6791–6801. https://doi.org/10.1093/jxb/erv385
Xiao M, Li Z, Zhu L, Wang J, Zhang B, Zheng F, Zhao B, Zhang H, Wang Y, Zhang Z (2021) The multiple roles of ascorbate in the abiotic stress response of plants: antioxidant, cofactor, and regulator. Front Plant Sci 12:598173. https://doi.org/10.3389/fpls.2021.598173
Yang TY, Huang WT, Zhang J, Yang LT, Huang ZR, Wu BS, Lai NW, Chen LS (2021) Raised pH conferred the ability to maintain a balance between production and detoxification of reactive oxygen species and methylglyoxal in aluminum-toxic Citrus sinensis leaves and roots. Environ Pollut 268:115676. https://doi.org/10.1016/j.envpol.2020.115676
Zhao X, Chen Q, Wang Y, Shen Z, Shen W, Xu X (2017) Hydrogen-rich water induces aluminum tolerance in maize seedlings by enhancing antioxidant capacities and nutrient homeostasis. Ecotoxicol Environ Saf 144:369–379. https://doi.org/10.1016/j.ecoenv.2017.06.045
Zhu XF, Lei GJ, Wang ZW, Shi YZ, Braam J, Li GX, Zheng SJ (2013) Coordination between apoplastic and symplastic detoxification confers plant aluminum resistance. Plant Physiol 162:1947–1955. https://doi.org/10.1104/pp.113.219147
Zobel RW (2008) Hardware and software efficacy in assessment of fine root diameter distributions. Comput Electron Agric 60:178–189. https://doi.org/10.1016/j.compag.2007.08.002
Acknowledgements
We are grateful to the Instituto de Biotecnologia Aplicada a Agropecuária (Bioagro) and the Núcleo de Microscopia e Microanálise (NMM) of the Universidade Federal de Viçosa (UFV) for providing the facilities for the conduction of the experiments and data analysis. The present work was carried out with the support of the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES)—Financing Code 001 and Fundação de Amparo à Pesquisa do Estado de Minas Gerais (FAPEMIG), and the Conselho Nacional de Desenvolvimento Científico Tecnológico (CNPq) (Process 306804/2020-4).
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Yoshida, C.H.P., Pacheco, A.C., de Marcos Lapaz, A. et al. Tolerance mechanisms to aluminum in popcorn inbred lines involving aluminum compartmentalization and ascorbate–glutathione redox pathway. Planta 257, 28 (2023). https://doi.org/10.1007/s00425-022-04062-3
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DOI: https://doi.org/10.1007/s00425-022-04062-3