Crop productivity is intimately linked to environmental conditions. For more than 11,000 years, humans have cultivated land to obtain food, and this cultivation is strongly dependent on rainfall, soil conditions, and temperature. New cultivation methods have improved throughout history, resulting in improved fruit production and quality and increased profitability. However, strong dependence on climatic conditions remains, and these conditions change with time, mostly due to the effects of human activity on Earth.
Global climate change is causing rapid variations in parameters such as soil and air temperature (Mellander et al., 2007). The rate of global warming is expected to continue increasing if no mitigation efforts are enabled (Teixeira et al., 2013). By 2080, it is expected that parameter values will reach record numbers in most cropping areas worldwide (Battisti and Naylor, 2009). Agricultural production and, consequently, food security, are strongly affected by temperature, which controls the rate of all metabolic processes leading to biomass and fruit and grain production (Hay and Walker, 1989). Moreover, high temperatures can increase the risk of drought, limit photosynthesis rates, and induce oxidative stress, and all of these negative effects are exacerbated in semi-arid and tropical areas. Of particular interest are the effects induced by short occurrences of extremely high temperatures, which are also known as heat stress (HS) events (Teixeira et al., 2013). Peaks of high temperatures, even when they occur for a few hours, may have dramatic effects on reduced crop production (Porter and Semenov, 2005). HS has both direct and indirect effects on plants, such as lower capacities for water acquisition, changes in Pi acquisition, metabolism, and homeostasis (Pacak et al., 2016), and severe damage to the plasma membrane of cells (Uemura et al., 2006; Zhu et al., 2017). Because HS events are likely to become more frequent with global warming (Tebaldi et al., 2006), it is important to find alternatives to protect crops under such situations.
Among agronomical practices introduced in semi-arid areas in the latest 30 years, the use of plastic greenhouses has become very popular and proved quite successful (Espí et al., 2006). Plastic increases production quality and quantity while reducing the consumption of valuable resources (such as water, pesticides, fertilizers, and energy). Plastics also retain CO2, protect from wind, and warm the soil, thereby preserving humidity and reducing the leaching of pesticides and fertilizers. When whitened with lime, plastics reduce radiation, thereby lowering temperature up to 5 to 8 °C and protecting plants, roots, and soil structures. Some estimates indicate that without plastics, 60% of all fruit and vegetable production in these semi-arid and fragile areas would be endangered. A southeastern Spanish province, Almeria, is paradigmatic in the use of whitened plastic greenhouses. With a total of ≈32,000 ha covered (Tierra y Mar, 2019), this “plastic sea” that can be seen even from orbital satellites has changed the economy and agronomical practices of the zone, thereby becoming the most important production area for fruits, vegetables, and horts of Europe and one of the most important in the world. Moreover, because crop cultivation is performed during two cycles per year for most products, the real surface of production of this area per year is 43,086 ha. Of these, three of the top agricultural crops are tomato (Solanum lycopersicum L., 11,081 ha), pepper (Capiscum annuum L., 9325 ha), and cucumber (Cucumis sativus L., 4839 ha), rendering total production values of more than 1 million t, 650,000 t, and 450,000 t per year, respectively (data provided by Consejería de Agricultura, Pesca y Desarrollo Rural, Junta de Andalucía, Spain, 2013). The total income generated in this area by using under-plastic agronomic practices has reached €2333.2 million. It is easy to understand that all types of innovative techniques improving production, crop protection, and environmental management are of enormous interest at this zone and, by extension, in all similar agricultural areas.
Another agronomical practice introduced recently is the biological management of agriculture by using macro- and microorganisms (e.g., to induce pollenization, control pests, or reduce water and fertilizer use), which has become a real revolution in the latest years. Among the microorganisms used, arbuscular mycorrhizal fungi (AMF) have been revealed to be crucial in all sustainable practices (Duhamel and Vandenkoornhuyse, 2013; Pagano et al., 2016). This group of soil-borne microscopic fungi establishes an intimate symbiotic relationship with the immense majority of plant roots so that colonized plants no longer have a simple root; instead, they have a new and powerful supra-organ called arbuscular mycorrhiza (AM) for nutrient uptake (Azcón-Aguilar and Bago, 1994). AM are formed by most of the economically important crops, and their functioning consists of bidirectional nutrient transfer between the plant and fungal partner; while the plant provides the fungus with the necessary C resources to overcome its obligate biotrophic nature, the fungus provides the plant with water and mineral and organic nutrients (especially P) very efficiently from the soil via fungal hyphae (Smith and Smith, 2012). Furthermore, AM formation implicates a whole series of changes in plant capacities including, among others, enhanced resistance against pathogens (Pozo et al., 2013) and better adaptation to extreme environments (contaminated soils, drought, extreme temperatures) (Abdel-Latef et al., 2016; Lenoir et al., 2016). As a consequence of this, important amelioration of the plant nutritional status and physiological equilibrium, higher yield, and healthier and more sustainable crop production are obtained (Baum et al., 2015).
Different studies have revealed the important role that AM may have in temperature stress alleviation (Mathur et al., 2018; Zhu et al., 2017). To briefly summarize, and focusing on HS, AM formation increases plant biomass, thereby reducing leaf browning, and has better water use efficiency, water retention capacity, and relative water content. Increased antioxidative enzyme production (such as superoxide dismutase, catalase, and ascorbate peroxidase) and the generation of osmotic-active compounds (such as proline, trehalose, and glomalin) lead to better preservation of the plasma membrane of AM plant cells, thus protecting vegetal tissues against HS. AM plants subjected to HS also have greatly increased photosynthetic rates, stomatal conductivity, leaf transpiration, photosystem II efficiency, concentrations of chlorophyll (a and b) and carotenoids, and photochemical potential. Together with an increased rate in C-metabolism gene expression, soluble sugar content, better P uptake efficiency, assimilation, and use, and enhanced metabolism of N (nitrate, ammonium, and amino acids), AM plants are best-positioned to endure HS and overcome its negative effects. Moreover, mitigation of negative effects of combined drought and HS have been recently reported (Duc et al., 2018). However, to the best of our knowledge, no reports have been generated regarding the impact of AM symbiosis on fruit production and quality under severe HS situations, which are the most interesting issues for any producer.
This study aimed to fulfill that gap by studying, under agronomic plastic greenhouse conditions, the impact of AM inoculation on a severe (>45 °C) HS episode maintained for 11 d for three agricultural crops of key importance to horticulture: tomato, pepper, and cucumber. To achieve this, an ultra-pure, in vitro–issued, gel-based AM inoculant (MYCOGEL) that has largely demonstrated its efficacy in horticultural and extensive crop production in Almeria (Spain) was tested.
Abdel-Latef, A.A. & Chaoxing, H. 2011 Arbuscular mycorrhizal influence on growth, photosynthetic pigments, osmotic adjustment and oxidative stress in tomato plants subjected to low temperature stress Acta Physiol. Plant. 33 1217 1225
Abdel-Latef, A.A., Hashem, A., Rasoot, S., Abd-Allah, E.F., Alqarawi, A.A., Egamberdieva, D., Jan, S., Anjum, N.A. & Ahmad, P. 2016 Arbuscular mycorrhizal symbiosis and abiotic stress in plants: A review J. Plant Biol. 59 407 426
Aroca, R., Bago, A., Sutk, M., Paz, J.A., Cano, C., Amodeo, G. & Ruíz-Lozano, J.M. 2009 Expression analysis of the first arbuscular mycorrhizal fungi aquaporin described reveals concerted gene expression between salt-stressed and non-stressed mycelium Mol. Plant Microbe Interact. 22 1169 1178
Atkin, O.K., Sherlock, D. & Fitter, A.H. 2009 Temperature dependence of respiration in roots colonized by arbuscular mycorrhizal fungi New Phytol. 182 189 199
Azcón-Aguilar, C. & Bago, B. 1994 Physiological characteristics of the host plant promoting un undisturbed functioning of the mycorrhizal symbiosis, p. 47–60. In: S. Gianinazzi and H. Schuepp (eds.). Impact of arbuscular mycorrhizas on sustainable agriculture and natural ecosystems. Birkhauser, Basel
Bago, B. & Cano, C. 2006 Application of arbuscular mycorrhizal fungi in vitro biofertilizers in agro-industries, p. 375–379. In: A. Méndez-Vilas (ed.). Modern multidisciplinary applied microbiology. Wiley-VCH, Weinheim
Bago, B., Azcón-Aguilar, C. & Piché, Y. 1997 Extraradical mycelium of arbuscular mycorrhizae: The concealed extension of roots, p. 502–505. In: H. Flores, J.P. Lynch, and D. Eissenstat (eds.). Radical biology: Advances and perspectives on the function of plant roots. Amer. Soc. Plant Physiol., University Park, PA.
Baon, J.B., Smith, S.E. & Alston, A.M. 1994 Phosphorus uptake and growth of barley as affected by soil temperature and mycorrhizal infection J. Plant Nutr. 17 479 492
Barrett, G., Campbell, C.D. & Hodge, A. 2014 The direct response of the external mycelium of arbuscular mycorrhizal fungi to temperature and the implications for nutrient transfer Soil Biol. Biochem. 78 109 117
Baum, C., El-Tohamy, W. & Gruda, N. 2015 Increasing the productivity and product quality of vegetable crops using arbuscular mycorrhizal fungi: A review Scientia Hort. 187 131 141
Bunn, R., Lekberg, Y. & Zabinski, C. 2009 Arbuscular mycorrhizal fungi ameliorate temperature stress in thermophilic plants Ecology 90 1378 1389
Cabral, C., Ravnskov, S. & Tringovska, I. 2016 Arbuscular mycorrhizal fungi modify nutrient allocation and composition in wheat (Triticum aestivum L.) subjected to heat-stress Plant Soil 408 1 396 406
Cano, C. & Bago, A. 2005 Inoculante aséptico de micorrización y procedimientos de aplicación en condiciones in vitro y ex vitro. Patent no. P200501878, Spain
Chen, S., Jin, W. & Liu, A. 2013 Arbuscular mycorrhizal fungi (AMF) increase growth and secondary metabolism in cucumber subjected to low temperature stress Scientia Hort. 160 222 229
Chen, X.Y., Song, F.B. & Liu, F.L. 2014 Effect of different arbuscular mycorrhizal fungi on growth and physiology of maize at ambient and low temperature regimes ScientificWorldJournal
Duc, N.H., Csintalan, Z. & Posta, K. 2018 Arbuscular mycorrhizal fungi mitigate negative effects of combined drought and heat stress on tomato plants Plant Physiol. Biochem. 132 297 307
Duhamel, M. & Vandenkoornhuyse, P. 2013 Sustainable agriculture: Possible trajectories from mutualistic symbiosis and plant neodomestication Trends Plant Sci. 18 597 600
Gavito, M.E., Olsson, P.A., Rouhier, H., Medina-Peñafiel, A., Jakobsen, I., Bago, A. & Azcón-Aguilar, C. 2005 Temperature constraints on the growth and functioning of root organ cultures with arbuscular mycorrhizal fungi New Phytol. 168 179 189
Gianinazzi, S. & Schuepp, H. 1994 Impact of arbuscular mycorrhizas on sustainable agriculture and natural ecosystems. Birkhauser, Basel
Gianinazzi, S., Gollotte, A. & Binet, M. 2010 Agroecology: The key role of arbuscular mycorrhizas in ecosystem services Mycorrhiza 20 519 530
Hay, R.K.M. & Walker, A.J. 1989 An introduction to the physiology of crop yield. Longman Scientific and Technical, NY
Hawkes, C.V., Hartley, I.P. & Ineson, P. 2008 Soil temperature affects carbon allocation within arbuscular mycorrhizal networks and carbon transport from plant to fungus Glob. Change Biol. 14 1181 1190
Hu, Y., Wu, S. & Sun, Y. 2015 Arbuscular mycorrhizal symbiosis can mitigate the negative effects of night warming on physiological traits of Medicago truncatula L Mycorrhiza 25 131 142
Luu, D.T. & Maurel, C. 2005 Aquaporins in a challenging environment: Molecular gears for adjusting plant water status Plant Cell Environ. 28 85 96
Martin, C.A. & Stutz, J.C. 2004 Interactive effects of temperature and arbuscular mycorrhizal fungi on growth, P uptake and root respiration of Capsicum annuum L Mycorrhiza 14 241 244
Martín, M., Rubio, A., Remesal, E., Cano, C. & Bago, A. 2018 Application of the ultimate Arbuscular Mycrrhizal inoculant MYCOGEL® in Japan: Results and prospects J. Integrated Field Sci. 15 31 40
Mathur, S., Sharma, M.P. & Jajoo, A. 2018 Improved photosynthetic efficacy of maize (Zea mays) plants with arbuscular mycorrhizal fungi (AMF) under high temperature stress J. Photochem. Photobiol. B 180 149 154
Matsubara, Y., Kayukawa, Y. & Fukui, H. 2000 Temperature-stress tolerance of asparagus seedling through symbiosis with arbuscular mycorrhizal fungus J. Jpn. Soc. Hort. Sci. 69 570 575
Matsubara, Y., Hirano, I. & Sassa, D. 2004 Alleviation of high temperature stress in strawberry plants infected with arbuscular mycorrhizal fungi Environ. Control Biol. 42 105 111
Maya, M.A. & Matsubara, Y. 2013 Influence of arbuscular mycorrhiza on the growth and antioxidative activity in cyclamen under heat stress Mycorrhiza 23 381 390
Mellander, P.E., Lofvenius, M.O. & Laudon, H. 2007 Climate change impact on snow and soil temperature in boreal Scots pine stands Clim. Change 85 179 193
Pacak, A., Barciszewska-Pacak, M., Swida-Barteczka, A., Kruszka, K., Sega, P., Milanowska, K., Jakobsen, I., Jamorlowski, A. & Szweykowska-Kulinska, J. 2016 Heat stress affects Pi-related genes expression and inorganic phosphate deposition/accumulation in barley Frontiers Plant Sci. 7 1 19
Pagano, M.C., Dantas, B.L., Weber, O.B., Correa, E.A., Tancredi, F.D., Duarte, N.F., Bago, A. & Cabello, M.N. 2016 Mycorrhizas in agroecosystems, p. 91–100. In: M.C. Pagano (ed.). Recent advances on mycorrhizal fungi (Fungal Biology). Springer International, Switzerland
Phillips, J.M. & Hayman, D.S. 1970 Improved procedures for clearing roots and staining parasitic and vesicular arbuscular mycorrhizal fungi for rapid assessment of infections Trans. Brit. Mycol. Soc. 55 158 161
Plouznikoff, K., Declerck, S. & Calonne-Salmon, M. 2016 Mitigating abiotic stress in crop plants by arbuscular mycorrhizal fungi, p. 341–400. In: C.M.F. Vos and K. Kazan (eds.). Belowground defence strategies in plants. Springer International, Switzerland
Pozo, M.J., Jung, S.C., Martínez-Medina, A., López-Ráez, J.A., Azcón-Aguilar, C. & Barea, J.M. 2013 Root allies: Arbuscular mycorrhizal fungi help plants to cope with biotic stresses. In: R. Aroca (ed.). Symbiotic endophytes. Soil biology, vol. 37. Springer, Berlin, Heidelberg
Smith, S.E. & Read, D.J. 2010 Mycorrhizal symbiosis. 3rd ed. Academic Press, London
Smith, S.E. & Smith, F.A. 2012 Fresh perspectives on the roles of arbuscular mycorrhizal fungi in plant nutrition and growth Mycologia 104 1 13
Smith, S.E., Facelli, E., Pope, S. & Smith, F.A. 2010 Plant performance in stressful environments: Interpreting new and established knowledge of the roles of arbuscular mycorrhizas Plant Soil 326 3 20
Teixeira, E.I., Fischer, G., van Velthuizen, H., Walter, C. & Ewert, F. 2013 Global hot-spots of heat stress on agricultural crops due to climate change Agr. For. Meteorol. 170 206 215
Tierra y Mar 2019 La superficie de invernaderos de Andalucía oriental crece un 1,7 %. 7 Jan. 2019. <http://www.juntadeandalucia.es/presidencia/portavoz/tierraymar/138208/invernaderos/plastico/agricultura/Andalucia/cultivo>
Zhu, X.C., Song, F.B. & Xu, H.W. 2010a Arbuscular mycorrhizae improves low temperature stress in maize via alterations in host water status and photosynthesis Plant Soil 331 129 137
Zhu, X.C., Song, F.B. & Xu, H.W. 2010b Influence of arbuscular mycorrhizae on lipid peroxidation and antioxidant enzyme activity of maize plants under temperature stress Mycorrhiza 20 325 332
Zhu, X.C., Song, F.B. & Liu, S.Q. 2011 Effects of arbuscular mycorrhizal fungus on photosynthesis and water status of maize under high temperature stress Plant Soil 346 189 199
Zhu, C., Song, F.B. & Liu, F.L. 2017 Arbuscular mycorrhizal fungi and tolerance of temperature stress in plants, p. 163–194. In: Q.S. Wu (ed.). Arbuscular mycorrhizas and stress tolerance of plants. Springer Nature, Singapore