Abstract
This work aimed to quantify the concentration of soluble amino acids, nitrogen (N) and Cd in the developing seeds of maize plants that were grown in Cd-contaminated soil from seed sowing to the reproductive stages. The specific activities and feedback inhibition properties of lysine (Lys) metabolic enzymes were also determined in developing seeds. The potential maize yield was depressed by Cd exposure. Cadmium concentration in plant organs followed the decreasing order: roots > stems = leaves > developing seeds (37.04, 1.95, 1.46 and 0.22 mg kg−1 Cd, respectively). The relatively low Cd concentration in the remained developing seeds was a result from root- and ear-mediated reductions of the Cd translocation in plants. Plants under Cd exposure presented developing seeds with an increased N concentration (up to 7%) when compared to control plants. Furthermore, the level of soluble amino acids (particularly histidine, glycine, tyrosine, methionine, isoleucine and valine) was increased in the developing seeds of Cd-treated plants. In addition, changes in the feedback properties of dihydrodipicolinate synthase (DHDPS), an enzyme from lysine metabolism, were observed in developing seeds. In conclusion, the current study showed that maternal plant exposure to Cd can alter the concentration of soluble amino acids and the behavior of Lys metabolic enzymes in developing seeds. This study provided not only new information about the influence of the long-term Cd exposure on plants, but also data about protective plant strategies against Cd toxicity.
References
Alaee S, Talaiekhozani A, Rezaei S, Alaee K, Yousefian E (2014) Cadmium and male infertility. J Infertil Reprod Biol 2:62–69
Angelovici R, Batushansky A, Deason N, Gonzalez-Jorge S, Gore MA, Fait A, DellaPenna D (2017) Network-guided GWAS improves identification of genes affecting free amino acids. Plant Physiol 173:872–886
Ata-Ul-Karim ST, Cang L, Wang Y, Zhou D (2020) Interactions between nitrogen application and soil properties and their impacts on the transfer of cadmium from soil to wheat (Triticum aestivum L.) grain. Geoderma 357:113923
Azevedo RA, Arruda P (2010) High-lysine maize: the key discoveries that have made it possible. Amino Acids 39:979–989
Azevedo RA, Arruda P, Turner WL, Lea PJ (1997) The biosynthesis and metabolism of the aspartate derived amino acids in higher plants. Phytochemistry 46:395–419
Azevedo RA, Damerval C, Landry J, Lea PJ, Bellato CM, Meinhardt LW, Le Guilloux M, Delhaye S, Toro AA, Gaziola SA, Berdejo BDA (2003) Regulation of maize lysine metabolism and endosperm protein synthesis by opaque and floury mutations. Eur J Biochem 270:4898–4908
Bieleski RL, Turner NA (1966) Separation and estimation of amino acids in crude plant extracts by thin-layer electrophoresis and chromatography. Anal Biochem 17:278–293
Carvalho MEA, Castro PRC, Azevedo RA (2020a) Hormesis in plants under Cd exposure: from toxic to beneficial element? J Hazard Mater 384:121434
Carvalho MEA, Castro PRC, Kozak M, Azevedo RA (2020b) The sweet side of misbalanced nutrients in cadmium-stressed plants. Ann Appl Biol 176:275–284
Carvalho MEA, Piotto FA, Franco MR, Rossi ML, Martinelli AP, Cuypers A, Azevedo RA (2019) Relationship between Mg, B and Mn status and tomato tolerance against Cd toxicity. J Environ Manage 240:84–92
Carvalho MEA, Piotto FA, Gaziola SA, Jacomino AP, Jozefczak M, Cuypers A, Azevedo RA (2018) New insights about cadmium impacts on tomato: plant acclimation, nutritional changes, fruit quality and yield. Food Energy Secur 7:e00131
Commission Regulation (2014) EU 2014 no. 488/2014 of 12 May 2014. Amending Regulation (EC) no 1881/2006 as regards maximum levels of cadmium in foodstuffs. Available from: https://www.fsai.ie/uploadedFiles/Reg488_2014.pdf. Accessed 23 Jan 2018
Dietrich CC, Bilnicki K, Korzeniak U, Briese C, Nagel KA, Babst-Kostecka A (2019) Does slow and steady win the race? Root growth dynamics of Arabidopsis halleri ecotypes in soils with varying trace metal element contamination. Environ Exp Bot 167:103862
Dubos C, Huggins D, Grant GH, Knight MR, Campbell MM (2003) A role for glycine in the gating of plant NMDA-like receptors. Plant J 35:800–810
Esalq—Escola Superior de Agricultura “Luiz de Queiroz” (2018) Climatological data series of “Luiz de Queiroz” campus at Piracicaba, SP, Brazil. Available from: https://www.leb.esalq.usp.br/posto/index.html. Accessed 23 Jan 2018
Fahad S, Hussain S, Saud S, Hassan S, Shan D, Chen Y, Deng N, Khan F, Wu C, Wu W, Shah F, Ullah B, Yousaf M, Ali S, Huang J (2015) Grain cadmium and zinc concentrations in maize influenced by genotypic variations and zinc fertilization. Clean: Soil, Air, Water 43:1433–1440
FAO—Food and Agriculture Organization of the United Nations (2018) Cereals & Grains. Available from: https://www.fao.org/in-action/inpho/crop-compendium/cereals-grains/en/. Accessed 15 Apr 2020
Fidalgo F, Freitas R, Ferreira R, Pessoa AM, Teixeira J (2011) Solanum nigrum L. antioxidant defence system isozymes are regulated transcriptionally and posttranslationally in Cd-induced stress. Environ Exp Bot 72:312–319
Frisch DA, Gengenbach BG, Tommey AM, Seliner JM, Somers DA, Myers DE (1991) Isolation and characterization of dihydrodipicolinate synthase from maize. Plant Physiol 96:444–452
Gallego SM, Pena LB, Barcia RA, Azpilicueta CE, Iannone MF, Rosales EP, Zawoznik MS, Groppa MD, Benavides MP (2012) Unravelling cadmium toxicity and tolerance in plants: insight into regulatory mechanisms. Environ Exp Bot 83:33–46
Gaziola SA, Alessi ES, Guimaraes PEO, Damerval C, Azevedo RA (1999) Quality protein maize: a biochemical study of enzymes involved in lysine metabolism. J Agric Food Chem 47:1268–1275
He YM, Fan XM, Zhang GQ, Li B, Li TG, Zu YQ, Zhan FD (2019) Effects of arbuscular mycorrhizal fungi and dark septate endophytes on maize performance and root traits under a high cadmium stress. S Afr J Bot. https://doi.org/10.1016/j.sajb.2019.09.018
Hédiji H, Djebali W, Belkadhi A, Cabasson C, Moing A, Rolin D, Brouquisse R, Gallusci P, Chaïbi W (2015) Impact of long-term cadmium exposure on mineral content of Solanum lycopersicum plants: consequences on fruit production. S Afric J Bot 97:176–181
Hendrix S, Iven V, Eekhout T, Huybrechts M, Pecqueur I, Horemans N, Keunen E, De Veylder L, Vangronsveld J, Cuypers A (2020) Suppressor of Gamma Response 1 modulates the DNA damage response and oxidative stress response in leaves of cadmium-exposed Arabidopsis thaliana. Front Plant Sci 11:366
Jaouani K, Karmous I, Ostrowski M, El Ferjani E, Jakubowska A, Chaoui A (2018) Cadmium effects on embryo growth of pea seeds during germination: investigation of the mechanisms of interference of the heavy metal with protein mobilization-related factors. J Plant Physiol 226:64–76
Järup L, Åkesson A (2009) Current status of cadmium as an environmental health problem. Toxicol Appl Pharmacol 238:201–208
Kabata-Pendias A (2011) Trace elements in soils and plants. CRC Press, Boca Raton
Kato FH, Carvalho MEA, Gaziola SA, Piotto FA, Azevedo RA (2020) Lysine metabolism and amino acid profile in maize grains from plants subjected to cadmium exposure. Sci Agric 77:e20180095
Kovačević V, Kádár I, Andrić L, Zdunić Z, Iljkić D, Varga I, Jović J (2019) Environmental and genetic effects on cadmium accumulation capacity and yield of maize. Czech J Genet Plant Breed 55:70–75
Kovacevic V, Vragolovic A (2011) Genotype and environmental effects on cadmium concentration in maize. J Life Sci 5:926–932
Kumpaisal R, Hashimoto T, Yamada Y (1987) Purification and characterization of dihydrodipicolinate synthase from wheat suspension cultures. Plant Physiol 85:145–151
Lux A, Martinka M, Vaculík M, White PJ (2011) Root responses to cadmium in the rhizosphere: a review. J Exp Bot 62:21–37
Małkowski E, Sitko K, Szopiński M, Gieroń Z, Pogrzeba M, Kalaji HM, Zieleźnik-Rusinowska P (2020) Hormesis in plants: the role of oxidative stress, auxins and photosynthesis in corn treated with Cd or Pb. Int J Mol Sci 21:2099
Melo LCA, Alleoni LRF, Carvalho G, Azevedo RA (2011) Cadmium and barium toxicity effects on growth and antioxidant capacity of soybean (Glycine max L.) plants, grown in two soil types with different physicochemical properties. J Plant Nutr Soil Sci 174:847–859
Norton GJ, Travis AJ, Danku JMC, Salt DE, Hossain M, Islam MR, Price AH (2017) Biomass and elemental concentrations of 22 rice cultivars grown under alternate wetting and drying conditions at three field sites in Bangladesh. Food Energy Secur 6:98–112
Pereira MP, Corrêa FF, Castro EM, Oliveira JPV, Pereira FJ (2017) Leaf ontogeny of Schinus molle L. plants under cadmium contamination: the meristematic origin of leaf structural changes. Protoplasma 254:2117–2126
Retamal-Salgado J, Hirzel J, Walter I, Matus I (2017) Bioabsorption and bioaccumulation of cadmium in the straw and grain of maize (Zea mays L.) in growing soils contaminated with cadmium in different environment. Int J Environ Res Public Health 14:1399
Rizwan M, Ali S, Qayyum MF, Ok YS, Zia-Ur-Rehman M, Abbas Z, Hannan F (2017) Use of maize (Zea mays L.) for phytomanagement of Cd-contaminated soils: a critical review. Environ Geochem Health 39:259–277
SAS Institute (2011) SAS/STAT user’s guide: version 9.3. Cary, SAS Institute
Sawidis T (2008) Effect of cadmium on pollen germination and tube growth in Lilium longiflorum and Nicotiana tabacum. Protoplasma 233:95–106
Schenck CA, Maeda HA (2018) Tyrosine biosynthesis, metabolism, and catabolism in plants. Phytochemistry 149:82–102
Sebastian A, Prasad MNV (2016) Modulatory role of mineral nutrients on cadmium accumulation and stress tolerance in Oryza sativa L. seedlings. Environ Sci Pollut Res 23:1224–1233
Sharma SS, Dietz KF (2006) The significance of amino acids and amino acid-derived molecules in plant responses and adaptation to heavy metal stress. J Exp Bot 57:711–726
Soares C, Carvalho MEA, Azevedo RA, Fidalgo F (2019) Plants facing oxidative challenges—a little help from the antioxidant networks. Environ Exp Bot 161:4–25
Stepansky A, Leustek T (2006) Histidine biosynthesis in plants. Amino Acids 30:127–142
Teklić T, Lončarić Z, Kovačević V, Singh BR (2013) Metallic trace elements in cereal grain—a review: How much metal do we eat? Food Energy Secur 2:81–95
Varisi VA, Medici LO, Van der Meer I, Lea PJ, Azevedo RA (2007) Dihydrodipicolinate synthase in opaque and floury maize mutants. Plant Sci 173:458–467
Vazquez A, Recalde L, Cabrera A, Groppa MD, Benavides MP (2020) Does nitrogen source influence cadmium distribution in Arabidopsis plants? Ecotoxicol Environ Saf 191:110163
Wang X, Gao Y, Feng Y, Li X, Wei Q, Sheng X (2014) Cadmium stress disrupts the endomembrane organelles and endocytosis during Picea wilsonii pollen germination and tube growth. PLoS ONE 9:e94721
Yu H, Zhang F, Wang G, Liu Y, Liu D (2013) Partial deficiency of isoleucine impairs root development and alters transcript levels of the genes involved in branched-chain amino acid and glucosinolate metabolism in Arabidopsis. J Exp Bot 64:599–612
Acknowledgements
The authors acknowledge São Paulo Research Foundation (FAPESP—Grant 2009/54676-0), which also provided scholarships to F.H.K.B (2012/23981-4) and M.E.A.C. (2013/15217-5 and 2015/26640-1). R.A.A. acknowledges Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq-Brazil, 303749/2016-4) for the research fellowship.
Author information
Authors and Affiliations
Contributions
RAA, FHK and FAP designed the experiment; FHK carried out the experiment; FHK and SAG performed analyses; all authors wrote, edited and reviewed the manuscript.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Additional information
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
Kato, F.H., Carvalho, M.E.A., Gaziola, S.A. et al. Maize plants have different strategies to protect their developing seeds against cadmium toxicity. Theor. Exp. Plant Physiol. 32, 203–211 (2020). https://doi.org/10.1007/s40626-020-00179-6
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s40626-020-00179-6