Physiological and Metabolic Effects of the Inoculation of Arbuscular Mycorrhizal Fungi in Solanum tuberosum Crops under Water Stress
Abstract
:1. Introduction
2. Results
2.1. Profiles and Concentrations of Phenolic Compounds
2.2. Overall Results
3. Discussion
4. Materials and Methods
4.1. Reagents
4.2. Samples
4.3. Identification and Quantification of Phenolic Compounds in Leaves
4.4. Total Phenols Determination by the Folin-Ciocalteu Method
4.5. Determination of Antioxidant Activity
4.6. Statistical Analysis
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
- Hamooh, B.T.; Sattar, F.A.; Wellman, G.; Mousa, M.A.A. Metabolomic and Biochemical Analysis of Two Potato (Solanum tuberosum L.) Cultivars Exposed to In Vitro Osmotic and Salt Stresses. Plants 2021, 10, 98. [Google Scholar] [CrossRef] [PubMed]
- Batool, T.; Ali, S.; Seleiman, M.F.; Naveed, N.H.; Ali, A.; Ahmed, K.; Abid, M.; Rizwan, M.; Shahid, M.R.; Alotaibi, M.; et al. Plant growth promoting rhizobacteria alleviates drought stress in potato in response to suppressive oxidative stress and antioxidant enzymes activities. Sci. Rep. 2020, 10, 16975. [Google Scholar] [CrossRef] [PubMed]
- Kroschel, J.; Mujica, N.; Okonya, J.; Alyokhin, A. Insect pests affecting potatoes in tropical, subtropical, and temperate regions. In The Potato Crop, 1st ed.; Campos, H., Ortiz, O., Eds.; Springer International Publishing: Berlin, Germany, 2020; pp. 251–306. [Google Scholar]
- Chacón-Cerdas, R.; Barboza-Barquero, L.; Albertazzi, F.J.; Rivera-Méndez, W. Transcription factors controlling biotic stress response in potato plants. Physiol. Mol. Plant Pathol. 2020, 112, 101527. [Google Scholar] [CrossRef]
- Liu, B.; Kong, L.; Zhang, Y.; Liao, Y. Gene and Metabolite Integration Analysis through Transcriptome and Metabolome Brings New Insight into Heat Stress Tolerance in Potato (Solanum tuberosum L.). Plants 2021, 10, 103. [Google Scholar] [CrossRef]
- Rykaczewska, K. The impact of high temperature during growing season on potato cultivars with different response to environmental stresses. Am. J. Potato Res. 2013, 4, 2386–2393. [Google Scholar] [CrossRef]
- Rensink, W.A.; Iobst, S.; Hart, A.; Stegalkina, S.; Buell, C.R. Gene expression profiling of potato responses to cold, heat, and salt stress. Funct. Integr. Genom. 2005, 5, 201–207. [Google Scholar] [CrossRef]
- Zlatev, Z.; Lidon, F.C. An overview on drought induced changes in plant growth, water relations and photosynthesis. Emir. J. Food Agric. 2012, 24, 57–72. [Google Scholar]
- Malhi, G.S.; Kaur, M.; Kaushik, P.; Alyemeni, M.N.; Alsahli, A.A.; Ahmad, P. Arbuscular mycorrhiza in combating abiotic stresses in vegetables: An eco-friendly approach. Saudi J. Biol. Sci. 2020, 28, 1465–1476. [Google Scholar] [CrossRef]
- Dasgupta, A.; Klein, K. Chapter 2—Methods for measuring oxidative stress in the laboratory. In Antioxidants in Food, Vitamins and Supplements; Academic Press: Cambridge, MA, USA, 2014; pp. 19–40. [Google Scholar]
- Parniske, M. Arbuscular mycorrhiza: The mother of plant root endosymbioses. Nat. Rev. Microbiol. 2008, 6, 763–775. [Google Scholar] [CrossRef]
- Prasad, R.; Bhola, D.; Akdi, K.; Cruz, C.; Sairam, K.V.S.S.; Tuteja, N.; Varma, A. Introduction to mycorrhiza: Historical development. In Mycorrhiza-Function, Diversity, State of the Art; Springer: Cham, Switzerland, 2017; pp. 1–7. [Google Scholar]
- Finlay, R.D. Ecological aspects of mycorrhizal symbiosis: With special emphasis on the functional diversity of interactions involving the extraradical mycelium. J. Exp. Bot. 2008, 59, 1115–1126. [Google Scholar] [CrossRef]
- Garg, N.; Chandel, S. Arbuscular mycorrhizal networks: Process and functions. In Sustainable Agriculture; Springer: Dordrecht, The Netherlands, 2011; Volume 2, pp. 907–930. [Google Scholar]
- Quiroga, G.; Erice, G.; Ding, L.; Chaumont, F.; Aroca, R.; Ruiz-Lozano, J.M. The arbuscular mycorrhizal symbiosis regulates aquaporins activity and improves root cell water permeability in maize plants subjected to water stress. Plant Cell Environ. 2019, 42, 2274–2290. [Google Scholar] [CrossRef]
- Chitarra, W.; Pagliarani, C.; Maserti, B.; Lumini, E.; Siciliano, I.; Cascone, P.; Schubert, A.; Gambino, G.; Balestrini, L.; Guerrieri, E. Insights on the impact of arbuscular mycorrhizal symbiosis on tomato tolerance to water stress. Plant Physiol. 2016, 171, 1009–1023. [Google Scholar] [CrossRef]
- Chandrasekaran, M. Arbuscular Mycorrhizal Fungi Mediated Enhanced Biomass, Root Morphological Traits and Nutrient Uptake under Drought Stress: A Meta-Analysis. J. Fungi 2022, 8, 660. [Google Scholar] [CrossRef]
- Yang, Y.; Tang, M.; Sulpice, R.; Chen, H.; Tian, S.; Ban, Y. Arbuscular mycorrhizal fungi alter fractal dimension characteristics of Robinia pseudoacacia L. seedlings through regulating plant growth, leaf water status, photosynthesis, and nutrient concentration under drought stress. J. Plant Growth Regul. 2014, 33, 612–625. [Google Scholar]
- Abbaspour, H.; Saeidi-Sar, S.; Afshari, H.; Abdel-Wahhab, M.A. Tolerance of mycorrhiza infected pistachio (Pistacia vera L.) seedling to drought stress under glasshouse conditions. J. Plant Physiol. 2012, 169, 704–709. [Google Scholar] [CrossRef]
- Yadav, B.; Jogawat, A.; Rahman, M.S.; Narayan, O.P. Secondary metabolites in the drought stress tolerance of crop plants: A review. Gene Rep. 2021, 23, 101040. [Google Scholar] [CrossRef]
- Jamwal, K.; Bhattacharya, S.; Puri, S. Plant growth regular mediated consequences of secondary metabolites in medicinal plants. J. Appl. Res. Med. Aromat. Plants 2018, 9, 26–38. [Google Scholar]
- Rodríguez-Pérez, C.; Gómez-Caravaca, A.M.; Guerra-Hernández, E.; Cerretani, L.; García-Villanova, B.; Verardo, V. Comprehensive metabolite profiling of Solanum tuberosum L. (potato) leaves by HPLC-ESI-QTOF-MS. Food Res. Int. 2018, 112, 390–399. [Google Scholar] [CrossRef]
- Drapal, M.; Farfan-Vignolo, E.R.; Gutierrez, O.R.; Bonierbale, M.; Mihovilovich, E.; Fraser, P.D. Identification of metabolites associated with water stress responses in Solanum tuberosum L. clones. Phytochemistry 2017, 135, 24–33. [Google Scholar] [CrossRef]
- Fritz, V.; Tereucán, G.; Santander, C.; Contreras, B.; Cornejo, P.; Ferreira, P.A.A.; Ruiz, A. Effect of Inoculation with Arbuscular Mycorrhizal Fungi and Fungicide Application on the Secondary Metabolism of Solanum tuberosum Leaves. Plants 2022, 11, 278. [Google Scholar] [CrossRef]
- Alarcón, S.; Tereucán, G.; Cornejo, P.; Contreras, B.; Ruiz, A. Metabolic and antioxidant effects of inoculation with arbuscular mycorrhizal fungi in crops of flesh-coloured Solanum tuberosum treated with fungicides. J. Sci. Food Agric. 2022, 102, 2270–2280. [Google Scholar] [CrossRef]
- Hura, T.; Grzesiak, S.; Hura, K.; Thiemt, E.; Tokarz, K.; Wędzony, M. Physiological and biochemical tools useful in drought-tolerance detection in genotypes of winter triticale: Accumulation of ferulic acid correlates with drought tolerance. Ann. Bot. 2007, 100, 767–775. [Google Scholar] [CrossRef]
- Nahuelcura, J.; Ruiz, A.; Gomez, F.; Cornejo, P. The effect of arbuscular mycorrhizal fungi on the phenolic compounds profile, antioxidant activity and grain yields in wheat cultivars growing under hydric stress. J. Sci Food Agric. 2022, 102, 407–416. [Google Scholar] [CrossRef]
- Wahab, A.; Abdi, G.; Saleem, M.H.; Ali, B.; Ullah, S.; Shah, W.; Mumtaz, S.; Yasin, G.; Muresan, C.C.; Marc, R.A. Plants’ Physio-Biochemical and Phyto-Hormonal Responses to Alleviate the Adverse Effects of Drought Stress: A Comprehensive Review. Plants 2022, 11, 1620. [Google Scholar] [CrossRef] [PubMed]
- Naeem, M.; Shahzad, K.; Saqib, S.; Shahzad, A.; Younas, M.; Afridi, M.I. The Solanum melongena COP1LIKE manipulates fruit ripening and flowering time in tomato (Solanum lycopersicum). Plant Growth Regul. 2022, 96, 369–382. [Google Scholar] [CrossRef]
- Hasanuzzaman, M.; Parvin, K.; Bardhan, K.; Nahar, K.; Anee, T.I.; Masud, A.A.C.; Fotopoulos, V. Biostimulants for the Regulation of Reactive Oxygen Species Metabolism in Plants under Abiotic Stress. Cells 2021, 10, 2537. [Google Scholar] [CrossRef] [PubMed]
- Mohammadi, E.; Fattahi, M.; Barin, M.; Ashrafi-Saeidlou, S. Arbuscular mycorrhiza and vermicompost alleviate drought stress and enhance yield, total flavonoid, rutin content, and antioxidant activity of buckwheat (Fagopyrum esculentum Moench). S. Afr. J. Bot. 2022, 148, 588–600. [Google Scholar] [CrossRef]
- Abdi, N.; van Biljon, A.; Steyn, C.; Labuschagne, M.T. Bread Wheat (Triticum aestivum) Responses to Arbuscular Mycorrhizae Inoculation under Drought Stress Conditions. Plants 2021, 10, 1756. [Google Scholar] [CrossRef]
- Baum, C.; El-Tohamy, W.; Gruda, N. Increasing the productivity and product quality of vegetable crops using arbuscular mycorrhizal fungi: A review. Sci. Hortic. 2015, 187, 131–141. [Google Scholar] [CrossRef]
- Coyago-Cruz, E.; Corell, M.; Moriana, A.; Hernanz, D.; Stinco, C.M.; Mapelli-Brahm, P.; Meléndez-Martínez, A.J. Effect of regulated deficit irrigation on commercial quality parameters, carotenoids, phenolics and sugars of the black cherry tomato (Solanum lycopersicum L.) ‘Sunchocola’. J. Food Compos. Anal. 2022, 105, 104220. [Google Scholar] [CrossRef]
- Mthembu, S.G.; Magwaza, L.S.; Mashilo, J.; Mditshwa, A.; Odindo, A. Drought tolerance assessment of potato (Solanum tuberosum L.) genotypes at different growth stages, based on morphological and physiological traits. Agric. Water Manag. 2022, 261, 107361. [Google Scholar] [CrossRef]
- Ben Jalloul, A.; Chaar, H.; Tounsi, M.S.; Abderrabba, M. Variations in phenolic composition and antioxidant activities of Scabiosa maritima (Scabiosa atropurpurea sub. maritima L.) crude extracts and fractions according to growth stage and plant part. S. Afr. J. Bot. 2022, 146, 703–714. [Google Scholar] [CrossRef]
- Wagg, C.; Hann, S.; Kupriyanovich, Y.; Li, S. Timing of short period water stress determines potato plant growth, yield and tuber quality. Agric. Water Manag. 2021, 247, 106731. [Google Scholar] [CrossRef]
- Hirut, B.; Shimelis, H.; Fentahun, M.; Bonierbale, M.; Gastelo, M.; Asfaw, A. Combining ability of highland tropic adapted potato for tuber yield and yield components under drought. PLoS ONE 2017, 12, e0181541. [Google Scholar] [CrossRef]
- Rashidi, S.; Yousefi, A.R.; Pouryousef, M.; Goicoechea, N. Total phenol, anthocyanin, and terpenoid content, photosynthetic rate, and nutrient uptake of Solanum nigrum L. and Digitaria sanguinalis L. as affected by arbuscular mycorrhizal fungi inoculation. Weed Biol. Manag. 2020, 20, 95–108. [Google Scholar] [CrossRef]
- Liu, H.; Bruce, D.R.; Sissons, M.; Able, A.J.; Able, J.A. Genotype-dependent changes in the phenolic content of durum under water-deficit stress. Cereal. Chem. 2018, 95, 59–78. [Google Scholar] [CrossRef]
- Vaher, M.; Matso, K.; Levandi, T.; Helmja, K.; Kaljurand, M. Phenolic compounds and the antioxidant activity of the bran, flour and whole grain of different wheat varieties. Procedia Chem. 2010, 2, 76–82. [Google Scholar] [CrossRef]
- Naikoo, M.I.; Dar, M.I.; Raghib, F.; Jaleel, H.; Ahmad, B.; Raina, A.; Naushin, F. Role and regulation of plants phenolics in abiotic stress tolerance: An overview. Plant Signal. Mol. 2019, 9, 157–168. [Google Scholar]
- Sharma, A.; Shahzad, B.; Rehman, A.; Bhardwaj, R.; Landi, M.; Zheng, B. Response of Phenylpropanoid Pathway and the Role of Polyphenols in Plants under Abiotic Stress. Molecules 2019, 24, 2452. [Google Scholar] [CrossRef]
- Parada, J.; Valenzuela, T.; Gómez, F.; Tereucán, G.; García, S.; Cornejo, P.; Ruiz, A. Effect of fertilization and arbuscular mycorrhizal fungal inoculation on antioxidant profiles and activities in Fragaria ananassa fruit. J. Sci. Food Agric. 2019, 99, 1397–1404. [Google Scholar] [CrossRef]
- Brito, I.; Goss, M.J.; Alho, L.; Brígido, C.; van Tuinen, D.; Félix, M.R.; Carvalho, M. Agronomic management of AMF functional diversity to overcome biotic and abiotic stresses-The role of plant sequence and intact extraradical mycelium. Fungal Ecol. 2019, 40, 72–81. [Google Scholar] [CrossRef]
- Santander, C.; Aroca, R.; Cartes, P.; Vidal, G.; Cornejo, P. Aquaporins and cation transporters are differentially regulated by two arbuscular mycorrhizal fungi strains in lettuce cultivars growing under salinity conditions. Plant Physiol. Biochem. 2021, 158, 396–409. [Google Scholar] [CrossRef]
- Zhang, B.; Murtaza, A.; Iqbal, A.; Zhang, J.; Bai, T.; Ma, W.; Hu, W. Comparative study on nutrient composition and antioxidant capacity of potato based on geographical and climatic factors. Food Biosci. 2022, 46, 101536. [Google Scholar] [CrossRef]
- Gholinezhad, E.; Darvishzadeh, R.; Moghaddam, S.S.; Popović-Djordjević, J. Effect of mycorrhizal inoculation in reducing water stress in sesame (Sesamum indicum L.): The assessment of agrobiochemical traits and enzymatic antioxidant activity. Agric. Water Manag. 2020, 238, 106234. [Google Scholar] [CrossRef]
- Ren, A.T.; Zhu, Y.; Chen, Y.L.; Ren, H.X.; Li, J.Y.; Kay Abbott, L.; Xiong, Y.C. Arbuscular mycorrhizal fungus alters root-sourced signal (abscisic acid) for better drought acclimation in Zea mays L. seedlings. Environ. Exp. Bot. 2019, 167, 103824. [Google Scholar] [CrossRef]
- Amine-Khodja, I.R.; Boscari, A.; Riah, N.; Kechid, M.; Maougal, R.T.; Belbekri, N.; Djekoun, A. Impact of Two Strains of Rhizobium leguminosarum on the Adaptation to Terminal Water Deficit of Two Cultivars Vicia faba. Plants 2022, 11, 515. [Google Scholar] [CrossRef]
- Bajraktari, D.; Bauer, B.; Zeneli, L. Antioxidant Capacity of Salix alba (Fam. Salicaceae) and Influence of Heavy Metal Accumulation. Horticulturae 2022, 8, 642. [Google Scholar] [CrossRef]
- Jiménez-Aspee, F.; Quispe, C.; Soriano, M.d.P.C.; Fuentes Gonzalez, J.; Hüneke, E.; Theoduloz, C.; Schmeda-Hirschmann, G. Antioxidant activity and characterization of constituents in copao fruits (Eulychnia acida Phil., Cactaceae) by HPLC–DAD–MS/MSn. Food Res. Int. 2014, 62, 286–298. [Google Scholar] [CrossRef]
- Du, Z.; Bramlage, W.J. Modified thiobarbituric acid assay for measuring lipid oxidation in sugar-rich plant tissue extracts. J. Agric. Food Chem. 1992, 40, 1566–1570. [Google Scholar] [CrossRef]
Method | Standard | Equation | R2 | DL | QL | LR |
---|---|---|---|---|---|---|
HPLC | Quercetin | y = 128319x − 22693 | 0.995 | 0.89 mg L−1 | 2.98 mg L−1 | 2.98–60 mg L−1 |
HPLC | Chlorogenic acid | y = 115567x − 7883 | 1.000 | 0.06 mg L−1 | 0.18 mg L−1 | 0.18–100 mg L−1 |
FOLIN | Gallic acid | y = 0.0009x + 0.005 | 0.999 | 7.69 mg L−1 | 25.60 mg L−1 | 25 to 500 mg L−1 |
TEAC | Trolox | y = 0.4186x + 0.0147 | 0.994 | 0.07 µmol L−1 | 0.21 µmol L−1 | 0.21 to 0.17 µmol L−1 |
DPPH | Trolox | y = 0.5739x + 0.0084 | 0.996 | 0.02 µmol L−1 | 0.07 µmol L−1 | 0.07 to 0.7 µmol L−1 |
CUPRAC | Trolox | y = 4.2617x + 0.0545 | 0.994 | 0.02 µmol L−1 | 0.07 µmol L−1 | 0.07 to 0.4 µmol L−1 |
FRAP | Trolox | y = 1.7195x + 0.1976 | 0.997 | 0.01 µmol L−1 | 0.04 µmol L−1 | 0.04 to 0.4 µmol L−1 |
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Valdebenito, A.; Nahuelcura, J.; Santander, C.; Cornejo, P.; Contreras, B.; Gómez-Alonso, S.; Ruiz, A. Physiological and Metabolic Effects of the Inoculation of Arbuscular Mycorrhizal Fungi in Solanum tuberosum Crops under Water Stress. Plants 2022, 11, 2539. https://doi.org/10.3390/plants11192539
Valdebenito A, Nahuelcura J, Santander C, Cornejo P, Contreras B, Gómez-Alonso S, Ruiz A. Physiological and Metabolic Effects of the Inoculation of Arbuscular Mycorrhizal Fungi in Solanum tuberosum Crops under Water Stress. Plants. 2022; 11(19):2539. https://doi.org/10.3390/plants11192539
Chicago/Turabian StyleValdebenito, Analía, Javiera Nahuelcura, Christian Santander, Pablo Cornejo, Boris Contreras, Sergio Gómez-Alonso, and Antonieta Ruiz. 2022. "Physiological and Metabolic Effects of the Inoculation of Arbuscular Mycorrhizal Fungi in Solanum tuberosum Crops under Water Stress" Plants 11, no. 19: 2539. https://doi.org/10.3390/plants11192539