Water availability and formation of propagules of arbuscular mycorrhizal fungi associated with sorghum
Introduction
The climatic projections show that semi-arid areas will be more affected due to climate change, promoting more severe drought (Bates et al., 2008). In semi-arid areas, the phenomenon of drought is frequent, requiring adaptations for coexistence and sustainable management of water for agriculture (Rockström et al., 2010). The use of biotechnological tools to maintain quality production, even under a limited water condition, is of utmost importance for these regions. Therefore, arbuscular mycorrhizal fungi (AMF) play an important role in this context. AMF occur in the soil and promote benefits to plants (Smith and Read, 2008), increasing the transport of water and nutrients through the mycelium (Egerton-Warburton et al., 2007, Ruth et al., 2011, Tobar et al., 1994) and consequently influencing the plant's water balance (Augé, 2001).
Improved water relations can promote higher growth potential and yield in mycorrhized plants, particularly under water-limited or nutrient-limited conditions (Jayne and Quigley, 2014). In addition, physiological and biochemical mechanisms of defense against injuries caused by the water stress are enhanced with mycorrhization, as increase in expression of genes that encode for aquaporins, which are proteins that channel the passage of water through the cell membrane (Uehlein et al., 2007), increase the stomatal conductance (Cho et al., 2006) and the concentration of solutes that promote osmotic adjustment in the cell (Bohnert and Jensen, 1996), among others.
On the other hand, the AMF effects depend on the level of water deficiency, because the water deficit should not affect AMF survival and growth. Few studies emphasize the effects of drought stress on the AMF propagule production, and the glomerospore constitute the most important infective propagules for the majority of AMF species (Smith and Read, 2008). Besides, the water availability in the soil can affect the production of glomerospores differently depending on the isolate of AMF. In the field contrasting results are observed, low water availability in the soil can reduce the AMF propagules production (Cui and Nobel, 1992) or increase of the glomerospores number and negatively affect the mycorrhizal colonization (Panwar et al., 2011). These differences in the number of glomerospores in the field can be related to the AMF species community composition, since the infectivity, persistence and formation of propagules vary with the AMF group (Klironomos and Hart, 2002).
Under experimental conditions, a gradual reduction of soil moisture over four weeks resulted in increased production of external mycelium and sporulation of Glomus intraradices Schenck & Smith (Neumann et al., 2009). However, in extreme drought conditions a reduction of AMF sporulation occurs, but an increase in the formation of propagules can additionally occur depending on the form and duration of water stress, which is influenced also by the host and fungal species (Augé, 2001).
The different responses of the AMF species in promoting plant growth under water stress may indicate that some isolates of AMF can be more efficient than others in this condition (Ruiz-Lozano et al., 1995), due to differences in their ability to absorb water from the soil (Marulanda et al., 2003). Furthermore, glomerospores with different nucleotypes can present distinct mycorrhizal efficiency (Angelard et al., 2010). Viera and Glenn (1990) suggested that adaptation of the AMF to adverse environmental conditions can also be related to the large amount of nuclei, and it was demonstrated that this number can vary between species of AMF (Hosny et al., 1998). Marleau et al. (2011) showed that the number of nuclei has a linear relationship with spore diameter, indicating also that the variation in number of nuclei can be related to spore maturity.
The nuclei show variation in the number and also can be genetically distinct within the same glomerospore (Kuhn et al., 2001). This genetic variability within populations of AMF should be considered for the development and selection of mycorrhizal inoculants because this would ensure the possibility of gene expression under different conditions (Sanders, 2004).
In the symbiosis between plants and AMF, water restriction can reduce mycorrhizal colonization (Manoharan et al., 2010, Manoharan et al., 2010), which can influence the production of spores and number of nuclei in a spore. Studies related to sporulation of AMF under conditions of water stress and the number of nuclei in the glomerospores are scarce, and it is important to understand some aspects of the fungal genetics to expand our understanding of this symbiosis (Sanders and Croll, 2010), in order to make more efficient use of AMF.
The knowledge about the effects of water restriction on the sporulation of species of AMF is of great importance to the selection of species better adapted to this condition, allowing for the AMF isolate to survive and promote the development of plant. In this study we addressed the influence of water availability on different aspects of the biology of AMF, testing the hypothesis that these fungi have distinct strategies regarding to production of glomerospores and other propagules under different levels of water availability. For this, isolates of Claroideoglomus etunicatum (W.N. Becker & Gerd.) Walker & Schüßler, Gigaspora albida N.C. Schenck & G.S. Sm. and Scutellospora heterogama (T.H. Nicolson & Gerd.) Walker & Sanders were tested in association with plants of Sorghum bicolor (L.) Moench var. Ponta Negra. The objective of this work was to test the hypothesis that water availability in the soil affects the sporulation of C. etunicatum, G. albida and S. heterogama, which can thus lead to modifications in the infective potential and number of nuclei in glomerospores of these species.
Section snippets
Soil characteristics
The soil used for the experiment was a sandy loam soil type upper layer of a Typic Haplustults according to the classification Soil Survey Staff (2010), with 769 g sand kg−1, 215 g silt kg−1 and 16 g clay kg−1, with the following chemical characteristics: pH 5.2; electrical conductivity 0.22 dS m−1; P = 3.4 mg kg−1; K+ = 87.5 mg kg−1; Ca2+ = 316.1 mg kg−1; Mg2+ = 60.8 mg kg−1; Na+ = 3.0 mg kg−1; and Al3+ = 8.9 mg kg−1; cation exchange capacity (CEC) = 5.24 cmolc dm−3. The soil was previously sterilized in an autoclave for two
Water availability and sporulation of AMF
The water availability in the soil affected sporulation (p < 0.05). In general, maintaining soil water at 55–75% of field capacity was favorable to the production of glomerospores of AMF. The G. albida isolate presented point of maximum sporulation at 75% of field capacity, while S. heterogama at 71%, as predicted by the regression equation (Fig. 1). The reduction in water availability from 75% to 25% decreased the sporulation of both G. albida and S. heterogama by 99%. On the other hand, in C.
Water availability and sporulation of AMF
The number of glomerospores was affected by water availability, with a reduction in sporulation with less water availability (50% and 25%) for two of the three isolates studied (Fig. 3). The reduction of sporulation may be associated with the long period in which the plants were kept under water stress, with low water levels (50% and 25%) for the proper development of the plant, which may have directly affected the mycorrhizal symbiosis. This fact was highlighted by Augé (2001) and Manoharan et
Conclusion
The AMF have distinct sporulation strategies under different levels of water availability. While the reduction in the availability of soil water reduces the sporulation of G. albida and S. heterogama, G. etunicatum is not affected, pointing out that the quantity of glomerospores of these fungi is not directly related to the infectivity potential of its inocula. The isolates present different number of nuclei in glomerospores, with no significant change in number within a species across water
Acknowledgements
The authors would like to thank: Facepe for providing a research grant (APQ-1265-2.03/10) and a PhD scholarship to EM Silva; CNPq for providing research grants (Proc. 559248/2009-1 and 562637/2010-9) and PQ fellowships to AMY Melo, LC Maia and NF Melo; Univasf and Embrapa Semi-arid for support. Thanks are also due to the anonymous reviewers for their suggestions.
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