Divergent root P uptake strategies of three temperate grassland forage species
Introduction
Temperate grasslands are affected by nutrient deficiency and this deficiency is one of the main limiting factors for forage production (Muir et al., 2011). This is the case of the grasslands of the Salado River Basin (Argentina), a typical area for beef cattle production in which soils exhibit low phosphorus (P) availability for plant growth (Sainz Rozas et al., 2012). In addition, perennial grasses predominate over other plant species, including native perennial legumes, a fact that seriously affects forage quality and productivity (Cahuépé, 2004).
Feasible alternatives to increase forage production include the selection of plant species adapted to grow under P-limiting conditions, P fertilization, and the use of soil microorganisms involved in P nutrition (Ikoyi et al., 2018). Plant strategies to achieve this include increasing P uptake by increasing the root mass fraction and specific root length, and by having a more highly branched root system (Pang et al., 2010; Jeffery et al., 2018). Another plant strategy to grow under P-limiting conditions is the association with soil microorganisms such as arbuscular mycorrhizal (AM) fungi, which can reduce the impact of P depletion in the rhizosphere and improve plant P nutrition (Smith and Read, 2008).
In most grassland and pasture soils over the world, P fertilization is necessary to obtain maximum forage yield (Muir et al., 2011). However, when P availability in the soil increases due to the fertilization, both AM root colonization and mycorrhizal growth response decrease in several plant species (Smith and Read, 2008; Jeffery et al., 2018), even if AM fungi can still be actively contributing to plant P uptake (Smith et al., 2004). The mycorrhizal growth responses depend on the C metabolic pathway of the host plant species, the AM fungal community, and different environmental factors such as soil P availability and moisture (Klironomos, 2003). Thus, a strategy to maintain AM root colonization and preserve the benefits of AM symbiosis on plant growth and P uptake under P-limiting conditions is to decrease the P doses added (Chippano et al., 2020; Fornara et al., 2020).
The main groups of forage species, i.e., legumes and grasses, and their C metabolic pathway play an important role in the dependence on AM to grow under P-limiting conditions. Most studies have demonstrated that the inoculation with AM fungi has better effects on the plant growth and P acquisition of legumes than on those of grasses (Tawaraya, 2003; Tran et al., 2019). This is because legumes have a lower ability to explore the soil and higher P requirements for growth than grasses (Tawaraya, 2003; Chippano et al., 2020). Grouping plants on the basis of functional traits such as their metabolic pathway (C3 vs C4) may help to improve predictions of plant responses to AM fungi (Hoeksema et al., 2018). In this sense, C4 grasses show greater response to AM fungi than C3 grasses and C3 grasses show a weak AM response despite of soil P availability (Hetrick et al., 1989; Řezáčová et al., 2018).
In grassland ecosystems, legumes may increase AM colonization in roots of neighboring plants, and thus, nutrient transport, alleviating soil P deficiencies (Xiao et al., 2019). In addition, legumes occupy a central role in grasslands because they are able to fix atmospheric N2 through rhizobia symbiosis (Temperton et al., 2007). In the Salado River Basin, one of the most important naturalized legumes is Lotus tenuis Waldst & Kit. This legume has high plasticity, high-quality forage production and ability to grow under P-limiting conditions (Mendoza and Pagani, 1997; Cahuépé, 2004). Besides, it is highly dependent on AM fungi and shows high percentage of AM root colonization in a wide range of P levels in the soil (Mendoza and Pagani, 1997; Castillo et al., 2013; Chippano et al., 2020).
Regarding grasses, Schedonorus arundinaceus (Schreb.) Dumort is likely the most important C3 forage grass in temperate grasslands of the world (Tîtei et al., 2019). In the Salado River Basin, this species is naturalized, produces high-quality pasture and tolerates soil with P-deficiency (Mendoza et al., 2016). Schedonorus arundinaceus has both a root system highly efficient for P uptake and low P requirements to grow (Tawaraya, 2003). Ayala Torales et al. (1998) showed that S. arundinaceus has lower specific P uptake than the legume Lotus corniculatus, but did not study whether this was due to the benefits of the AM association on the legume. In the present work, we especially evaluate the role of the AM association on specific P uptake of S. arundinaceus and L. tenuis.
Another forage species recently introduced in the Salado River Basin is Panicum coloratum L. This species is a C4 grass with high productivity and adaptability to the environmental conditions, including the P-limiting conditions of this basin (Otondo et al., 2019). Panicum coloratum has been found to respond strongly to P fertilization and to show moderate AM root colonization growing in P-deficient soils (Chippano et al., 2020). The three forage species have a high agronomic value; however little is known about the effect of P fertilization on the mycorrhizal growth response and P uptake strategies of L. tenuis, S. arundinaceus and P. coloratum in symbiosis with native AM fungi from temperate grasslands, and especially from the Salado River Basin.
AM fungi are of high value for the functioning and sustainability of grasslands. Thus, both the AM symbiosis and a reduction in the amount of P fertilizer applied are sustainable strategies to increase forage production (Fornara et al., 2020). The AM symbiosis and the factors that regulate this association have been little studied in grassland soils, especially in those of the Salado River Basin. Thus, knowledge of the effect of both low and high levels of P fertilization and association with native AM fungi on the growth of legumes and C3 and C4 grasses is valuable information to take advantage of the benefits provided by native AM fungal communities.
Based on all the above, the aim of this study was to investigate the combined effect of a low and high-P dose and association with native AM fungi from the Salado River Basin on the development of three test plants of the main groups of forage species: a legume, L. tenuis, and two grasses with different C metabolic pathway, S. arundinaceus (C3) and P. coloratum (C4). We specifically aimed to test the following hypotheses: (1) the growth and P uptake of the legume increase by the interaction of P fertilization and AM fungi, whereas the development of C3 and C4 grasses is improved only by P addition, and (2) legume and C3 and C4 grasses show different strategies to increase P uptake under P-limiting conditions, mainly related to the association with native AM fungi in L. tenuis, to changes in root traits (specific root length and root mass fraction) in S. arundinaceus, and to a combination of both strategies in P. coloratum.
Section snippets
Experimental set up
The experiment was conducted using a factorial arrangement with a completely randomized design. The main factors were P fertilization (three levels: unfertilized, low and high doses) and native AM fungi (two levels: with and without AM fungi). Four replicates were assigned to each combination of P fertilization and AM treatment. Soil was collected from the top 0.15 m layer of a grassland of the Salado River Basin (35°37′S, 58°50′W, Province of Buenos Aires, Argentina). The climate is temperate
Plant yield
The shoot DW of L. tenuis was affected by P addition, AM fungi and the interaction of both factors (Fig. 1a; Table S2). The shoot DW of L. tenuis plants with P addition (both levels) and AM fungi increased, whereas that of plants without P addition and without and with AM fungi was 1.97 g. pot−1 and 5.57 g. pot−1, respectively. The highest value was achieved with the combination of high-P dose and AM fungi. Its shoot DW without P addition and with AM fungi was the same as that achieved by
Plant yield and mycorrhizal response
Phosphorous fertilization, the use of plant species adapted to grow under P-deficient conditions and AM symbiosis are alternatives that, either individually or combined, allow increasing forage production in temperate regions. For L. tenuis, AM fungi caused an increase in biomass yield similar to that obtained with only the addition of a low P dose. The ability of AM fungi to explore a greater volume of soil than the root system and absorb P beyond the limits of the P depletion zone (Smith and
Conclusions
The results of this work showed that the interaction of P addition and AM fungal communities increased L. tenuis biomass production because of its higher P requirement to grow and lower ability for P uptake than grasses. The presence of L. tenuis and the addition of low-P doses would improve forage quality and nutrient cycling with the maintenance of AM symbiosis and its benefits in temperate grasslands. The species studied showed different strategies for P uptake under P-limiting conditions.
Declaration of competing interest
The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
Acknowledgements
We thank the financial support by Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET, Argentina) (PIP 0950). We also thank María Victoria Gonzalez Eusevi for revising and editing the English of the manuscript.
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