Elsevier

Field Crops Research

Volume 240, 1 July 2019, Pages 106-115
Field Crops Research

Nutritional and environmental effects on biological nitrogen fixation in soybean: A meta-analysis

https://doi.org/10.1016/j.fcr.2019.05.006Get rights and content

Highlights

  • Soybean N2 fixation was reduced by N fertilization, water stress, and flooding.

  • Nitrogen effects were more detrimental in greenhouse than in field conditions.

  • Nutrients other than nitrogen and CO2 enrichment increased BNF.

  • Timing rather than magnitude of stress is critical in determining effects on BNF.

  • A unique mechanism might be controlling both nutrient and environmental effects on BNF.

Abstract

Biological N2 fixation (BNF) and mineral soil absorption are complementary N sources for soybean growth. BNF is sensitive to nutrient and environmental conditions, though a comprehensive synthesis of the studies underlying these conclusions is currently lacking. Our objective was to conduct a meta-analysis of nutrient and environmental effects on BFN. Articles reporting manipulative treatments and BNF estimations were compiled, and data and metadata were extracted. N fertilization reduced BNF ∼70% relative to the unfertilized control in greenhouse experiments and ∼44% in field experiments. This effect was higher for vegetative than for reproductive stage applications. Fertilization with other nutrients stimulated BNF relative to the unfertilized treatments. Water stress reduced BNF 40% relative to the unstressed control. The negative impact of water stress was larger when stress was applied at vegetative (-70%) compared to reproductive (-30%) stages. Flooding reduced BNF by 40% relative to the non-flooded control with highest effect when applied during vegetative stage (-82%). Increased temperature reduced BNF nitrogenase activity. Carbon dioxide enrichment has a stimulatory effect on BNF. With the exception of N fertilization, soybean and Rhizobium fitness showed a high positive correlation across nutrients and environmental factors. This work summarizes for the first time the impact and relative response of BNF to different nutrient and environmental factors. Results showed an initial critical stage (i.e. vegetative stage) for BNF that is common to most environmental factors negatively affecting BNF. This suggests that common strategies might exist to increase BNF that are independent of the specific identity of the stressor. Also, the positive correlation between host and Rhizobium fitness suggest that strategies to increase BNF potential are the same that those required to increase crop performance. We observed publication bias for some variables, suggesting that effect sizes might be inflated compared to true effect sizes. The only way to solve this problem is to find venues for publication of no significant results when sound experimental approaches and reasonable statistical power can be proved.

Introduction

Nitrogen (N) is usually the most limiting nutrient for crop productivity (Vitousek and Howarth, 1991). Despite the high N content in the atmosphere, N is not present in soil parent material (Hedin et al., 2009). Therefore, soil N inputs to the biosphere relies on organic matter, synthetic fertilizer applications, and biological N2 fixation (BNF) via nitrogenase enzyme activity (Galloway et al., 2008; Vitousek et al., 2013). Biological fixation is accomplished in part by some blue-green algae, but predominantly by free-living or symbiotic bacteriae. The last group (i.e. Rhizobia) establish a mutualistic association with legumes species, fixing N from the atmosphere that is used by both the bacteria and the host (Herridge et al., 2008). Rhizobia fixes more than 30 × 109 kg N every year in 250 million hectares worldwide under legume cultivation, (Kinzig and Socolow, 1994) and is predicted to increase to 50 × 109 kg N year−1 by 2050 (Galloway et al., 2004). Global legume cultivation is dominated by soybean, a key component of global human and livestock diet (Brumm and Hurburgh, 1990).

Soybean seed yield is positively correlated with total N uptake (Salvagiotti et al., 2008; Rotundo et al., 2014; Santachiara et al., 2017), and 44–72% is usually accounted by BNF (Ciampitti and Salvagiotti, 2018). Maximum BNF occurs when the seed filling period begins (increasing seed demand) and decreases through physiological maturity (Zapata et al., 1987). Even though fixation provides a high proportion of total N demand, high rates of BNF are usually not required to maximize soybean seed yield in soils with adequate mineral N supply because of a trade-off between both N sources (Santachiara et al., 2017). However, high rates of BNF are necessary to maximize yields in soils with low to medium N fertility and to reach near-to-neutral soil N balances after soybean cultivation (Collino et al., 2015; Santachiara et al., 2017). In this context, understanding the factors affecting BNF is especially relevant for both soybean production and long term sustainability of agriculture.

Biological N2 fixation is considered an extremely sensitive process influenced by nutrient and environmental conditions (Graham, 1992; Purcell et al., 1998; Zahran, 1999; King and Purcell, 2005; Liu et al., 2011). There are several published studies focused on quantifying the effect of multiple factors on BNF. Previous reports have shown that BNF is reduced by high soil nitrate availability (Eaglesham et al., 1983; Vessey and Waterer, 1992; Arrese-lgor et al., 1997), soil water deficit (Minchin and Pate, 1975; Bennett and Albrecht, 1984; Sall and Sinclair, 1991), and long periods of soil water saturation (Rajaramamohan-Rao, 1976; Bennett and Albrecht, 1984;). Likewise, departures from temperatures ranging from 22 to 25 °C resulted in reductions in BNF (Lindemann and Ham, 1979). Non-optimal temperatures, water stress, high soil N availability, and soil pH have been reported to have inhibitory effects (Sprent, 1971; Pankhurst and Sprent, 1975; Munévar and Wollum, 1981; Graham, 1992; Bordeleau and Prévost, 1994; Zhang et al., 1996; Zahran, 1999; Hungria and Vargas, 2000; Prudent et al., 2016). In contrast, radiation, carbon dioxide concentration (Murphy, 1986), and nutrient availability have been reported to have enhancing effects (Graham, 1992; Zahran, 1999; Divito and Sadras, 2014). While the relationship between these factors and BNF has been analyzed before, a quantitative appraisal summarizing effect sizes and factors affecting these effect sizes is currently lacking. Previous meta-analysis on N, P, K, and S effects on soybean (Divito and Sadras, 2014) focused on mostly on nodulation (both number and weight) but not on direct estimations of BNF as in the present study.

Meta-analyses are designed to integrate information from various experiments and conditions evaluating common treatment effects (Curtis and Wang, 1998). Meta-analyses are particularly informative since they provide effect sizes estimates, calculated as the response of a treatment relative to an untreated control. Different meta-analysis has been successfully used to estimate effects of environmental conditions of soybean seed quality (Rotundo and Westgate, 2009), soybean responses to increases in CO2 (Ainsworth et al., 2002), and ozone concentration (Morgan et al., 2003). Using this approximation, we seek to summarize and quantify overall soybean BNF responses to environmental and nutritional variables. Therefore, the objective of this study was to perform a meta-analysis summarizing published data regarding the effect of nutrient addition and environmental variation on soybean BNF. Interactions among treatment timing, rate and intensity were also explored.

Section snippets

Database compilation and treatments partitioning

Published articles about soybean BNF were searched using Scopus®, Science Direct® and Google Scholar® databases of peer reviewed literature. Employed search criteria included a hierarchy structure: (a) soybean as object of study (“common” and/or “scientific name”), (b) nutrient (application or fertilization) and environmental condition (e.g. water deficit) as intervention (various synonymous were used for each search, for instance “water stress" or “drought” or "water deficit" or "water

Response of BNF to nutrient addition

For the unweighted analysis, N fertilization reduced BNF by 49% and by 70% as estimated for NDFA and ARA, respectively (Fig. 1a). Relative reduction in NDFA was 44% in field experiments while it was more than 70% in greenhouse experiments (Qt = 17.2; P < 0.001; Sup. Table I.1). This difference between experimental setting was not observed when BNF was estimated as ARA (Qt = 0.4; n.s.). Increased rate of N application in field experiments reduced BNF when estimated by both NDFA and ARA (Fig. 1b;

Discussion

Biological N2 fixation has been reported as a very sensitive process affected by several environmental factors. Even when the relative impact of N nutrition on soybean BNF has been extensively analyzed (Salvagiotti et al., 2008; Ciampitti and Salvagiotti, 2008), the effects of other environmental conditions and nutrients other than N, has not been extensively summarized. The current meta-analysis integrates numerous data sources to attain general response patterns of BNF to soil nutrient

Conclusions

The current meta-analysis reported the different effects of nutrient availability and environmental factors on BNF in soybean. Results from this work would serve as possible starting point for generating new insights and additional hypotheses regarding BNF. Environmental (water deficiency, flooding and temperature) and N addition during initial vegetative stages had the most detrimental effects of BNF. This pattern might be extended to other factors affecting negatively BNF not analyzed here.

Acknowledgments

This research was partially funded by Agencia Nacional de Promoción Científica y Tecnológica, Argentina (PICT2011-1292). Authors wanted to thanks Ryan McCormick for insightful comments on the manuscript. G. Santachiara & J.L. Rotundo are members of CONICET, The Argentina National Research Council.

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