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Showing papers in "Biology and Fertility of Soils in 2015"


Journal ArticleDOI
TL;DR: Several pieces of evidence highlight that the inoculation of plants with PGPR can have considerable effects on plant at both physiological and molecular levels, suggesting the possibility that soil biota could stimulate plants being more efficient in retrieving nutrients from soil and coping with abiotic stresses.
Abstract: Plant growth-promoting rhizobacteria (PGPR) are soil bacteria that are able to colonize rhizosphere and to enhance plant growth by means of a wide variety of mechanisms like organic matter mineralization, biological control against soil-borne pathogens, biological nitrogen fixation, and root growth promotion. A very interesting feature of PGPR is their ability of enhancing nutrient bioavailability. Several bacterial species have been characterized as P-solubilizing microorganisms while other species have been shown to increase the solubility of micronutrients, like those that produce siderophores for Fe chelation. The enhanced amount of soluble macro- and micronutrients in the close proximity of the soil-root interface has indeed a positive effect on plant nutrition. Furthermore, several pieces of evidence highlight that the inoculation of plants with PGPR can have considerable effects on plant at both physiological and molecular levels (e.g., induction of rhizosphere acidification, up- and downregulation of genes involved in ion uptake, and translocation), suggesting the possibility that soil biota could stimulate plants being more efficient in retrieving nutrients from soil and coping with abiotic stresses. However, the molecular mechanisms underlying these phenomena, the signals involved as well as the potential applications in a sustainable agriculture approach, and the biotechnological aspects for possible rhizosphere engineering are still matters of discussion.

564 citations


Journal ArticleDOI
TL;DR: In this article, a more deliberate adoption of knowledge of plant physiological processes is proposed to identify the physicochemical "packaging" of nutrients, their composition, amount and timing of application to meet plant physiological needs for improved instantaneous uptake.
Abstract: Meeting human needs within the ecological limits of our planet calls for continuous reflection on, and redesigning of, agricultural technologies and practices. Such technologies include fertilisers, the discovery and use of which have been one of the key factors for increasing crop yield, agricultural productivity and food security. Fertiliser use comes, however, at an environmental cost, and fertilisers have also not been a very economically effective production factor to lift many poor farmers out of poverty, especially in African countries where application on poor soils of unbalanced compositions of nutrients in fertilisers has shown limited impact on yield increase. Agronomic practices to apply existing mineral fertilisers, primarily containing N, P and K, at the right time, the right place, in the right amount, and of the right composition can improve the use efficiency of fertilisers. However, the overall progress to reduce the negative side effects is inadequate for the desired transformation toward sustainable agriculture in poor countries. Globally, there have been no fundamental reflections about the role and functioning of mineral fertilisers over the past 5 decades or more, and compared to other sectors, dismal investments have been made in mineral fertiliser research and development (R&D). In this paper, we reflect on current fertilisers and propose a more deliberate adoption of knowledge of plant physiological processes—including the diversity of mineral nutrient uptake mechanisms, their translocation and metabolism—as an entry point in identifying the physicochemical “packaging” of nutrients, their composition, amount and timing of application to meet plant physiological needs for improved instantaneous uptake. In addition to delivery through the root, we suggest that efforts be redoubled with several other uptake avenues, which as of now are at best haphazard, for the delivery of nutrients to the plant, including above ground parts and seed coating. Furthermore, ecological processes, including nutrient-specific interactions in plant and soil, plant-microorganism symbiosis, and nanotechnology, have to be exploited to enhance nutrient uptake. It is hoped that concerted R&D efforts will be pursued to achieve these strategies.

276 citations


Journal ArticleDOI
TL;DR: In this article, the impacts of nitrogen (N) addition, phosphorus (P) addition and N×P interaction on soil microbial biomass and microbial community composition in tropical forests were explored, and it was shown that N addition usually did not affect microbial biomass, which was increased by P addition over 3 years of fertilization.
Abstract: Nutrient availability greatly regulates soil microbial processes and functions in tropical forests. However, few studies have explored the impacts of nitrogen (N) addition (100 kg P ha−1 year−1), phosphorus (P) addition (100 kg N ha−1 year−1), and N × P interaction on soil microbial biomass and microbial community composition in tropical forests. We established a field nutrient manipulation experiment in a secondary tropical forest of South China. Soil physicochemical properties and microbial community composition were measured. Analysis of phospholipid fatty acids (PLFAs) was used to determine soil microbial biomass and composition, and both were related to environmental factors by the redundancy analysis (RDA) and principal response curves (PRC). We demonstrated that N addition usually did not affect microbial biomass, which was increased by P addition over 3 years of fertilization. Nitrogen addition decreased soil bacterial biomass but did not affect soil fungal biomass after 3 years of fertilization. After P addition, soil fungal biomass increased faster than soil bacterial biomass, indicating a more sensitive response of soil fungi to P addition than bacteria. Phosphorus addition increased fungi/bacteria ratio (F/B) ratios after 3 years of fertilization. Both N and P additions had different effects on soil microbial community in this tropical forest and, thus, probably altered ecosystem functioning.

165 citations


Journal ArticleDOI
TL;DR: 2 years of biofertilizer application manipulated the composition of rhizosphere microbial community and induced the Fusarium suppression by increasing bacterial diversity and potentially stimulating microbial consortia taxa, such as Acidobacteria (Gp1 and Gp3), Firmicutes, Leptosphaeria, and Phaeosphaeriopsis.
Abstract: In our previous work, applying biofertilizer containing Bacillus amyloliquefaciens strain NJN-6 to a banana orchard infected by a serious Fusarium wilt disease over two consecutive years effectively controlled this soil-borne disease. In this study, deep pyrosequencing of 16S ribosomal RNA (rRNA) genes and internal transcribed spacer (ITS) sequences was performed to investigate how the composition of rhizosphere microbial community responded to the application of biofertilizer (BIO), pig manure compost (PM), and chemical fertilizer (CF) and to explore the potential correlation between the microbial community composition and the Fusarium wilt disease. A total of 104,201 bacterial 16S rRNA genes and 154,953 fungal ITS sequence reads were obtained after basic quality control, and Acidobacteria, Actinobacteria, Bacteroidetes, Firmicutes, Proteobacteria, and Ascomycota were the most abundant bacterial and fungal phyla across all samples. Compared with the PM and CF control, the alpha diversity of bacteria significantly (P < 0.05) increased, whereas the value of the fungi was significantly (P < 0.05) reduced following two consecutive years of biofertilizer application. Moreover, the abundance of Acidobacteria (Gp1 and Gp3), Firmicutes, Leptosphaeria, and Phaeosphaeriopsis was significantly (P < 0.05) increased, while the abundance of Proteobacteria and Ascomycota was significantly (P < 0.05) decreased in the BIO treatment. Furthermore, the abundance of Fusarium, a causal pathogen for Fusarium wilt disease, was significantly (P < 0.05) reduced in the BIO treatment compared with the CF control and was slightly reduced (not significant) compared with the PM control. Interestingly, the disease incidence was negatively correlated with the enriched taxa of Acidobacteria (Gp1 and Gp3) and Firmicutes, Leptosphaeria, and Phaeosphaeriopsis but positively correlated with abundance of Proteobacteria, Ascomycota, Fusarium, Cylindrocarpon, Gymnascella, Monographella, Pochonia, and Sakaguchia taxa. The results from this study suggest that 2 years of biofertilizer application manipulated the composition of rhizosphere microbial community and induced the Fusarium suppression by increasing bacterial diversity and potentially stimulating microbial consortia taxa, such as Acidobacteria (Gp1 and Gp3), Firmicutes, Leptosphaeria, and Phaeosphaeriopsis.

155 citations


Journal ArticleDOI
TL;DR: In this paper, the effects of maize straw biochar on phosphorus availability in two soils with different P sorption capacities (iron and aluminum dominated slight acid Red earth and calcium dominated alkaline Fluvo-aquic soil).
Abstract: This study investigated the effects of maize (Zea mays L.) straw biochar on phosphorus (P) availability in two soils with different P sorption capacities (iron and aluminum dominated slight acid Red earth and calcium dominated alkaline Fluvo-aquic soil). A 42-day incubation experiment was conducted to study how applications of biochar at different rates (0, 2, 4, and 8 % soil, w/w), in combination with and without mineral KH2PO4 fertilizer, affected contents of soil Olsen-P and soil microbial biomass P (SMB-P) and phosphomonoesterase activity. In addition, P sorption characteristics of soils amended with biochar, as well as main properties of the biochar and the soils, were determined. Application of 8 % biochar after 42 days of incubation substantially increased soil Olsen-P from 3 to 46 mg kg−1 in Red earth and from 13 to 137 mg kg−1 in Fluvo-aquic soil and increased SMB-P from 1 to 9 mg kg−1 in Red earth and from 9 to 21 mg kg−1 in Fluvo-aquic soil. The increase was mainly due to high concentrations of P in the ash fraction (77 % of total biochar P). Biochar effect on soil Olsen-P and SMB-P increased by higher biochar application rates and by lower P sorption capacity. Biochar application significantly reduced acid phosphomonoesterase activity in Red earth and alkaline phosphomonoesterase activity in Fluvo-aquic soil due to large amount of inorganic P added. We conclude that maize straw biochar is promising to potentially improve soil P availability in low-P soils, but further research at field scale is needed to confirm this.

139 citations


Journal ArticleDOI
TL;DR: Overall, the data suggest that conversion of rainforests into production systems results in more pronounced changes in microbial community composition in soil as compared to litter, and redundancy analysis indicated that soil pH explained most of the variation in soil microbialcommunity composition.
Abstract: Focusing on Sumatra, a hotspot of tropical lowland rainforest transformation, we investigated effects of the con- version of rainforests into rubber agroforests (Bjungle rubber^), intensive rubber, and oil palm plantations on the communities of litter and soil microorganisms and identified factors responsible for these changes. Litter basal respiration, microbial biomass, total bacterial phospholipid fatty acids (PLFAs), and fungal PLFAs did not vary significantly with rainforest conversion. In litter of converted ecosystems, the concentration of certain PLFAs including the Gram-negative bacteria marker PLFA cy17:0 and the Gram-positive bacteria marker PLFA i17:0 was reduced as compared to rainforest, whereas the concentration of the arbuscular mycorrhizal fungi (AMF) marker neutral lipid fatty acid (NLFA) 16:1ω5c in- creased. As indicated by redundancy analysis, litter pH and carbon concentration explained most of the variation in litter microbial community composition. In soil, microbial biomass did not vary significantly with rainforest conversion, whereas basal respiration declined. Total PLFAs and especially that of Gram-negative bacteria decreased, whereas PLFA i17:0 in- creased with rainforest conversion. The concentration of fun- gal PLFAs increased with rainforest conversion, whereas NLFA 16:1ω5c did not change significantly. Redundancy analysis indicated that soil pH explained most of the variation in soil microbial community composition. Overall, the data suggest that conversion of rainforests into production systems results in more pronounced changes in microbial community composition in soil as compared to litter. In particular, the response of fungi and bacteria was more pronounced in soil, while the response of AMF was more pronounced in litter. Notably, only certain bacterial markers but not those of saprotrophic fungi and AMF were detrimentally affected by rainforest conversion.

111 citations


Journal ArticleDOI
TL;DR: In this paper, the effects of short-term (less than 2 years) conservation managements on top soil microbial community composition and soil organic C (SOC) fractions under a rice-wheat rotation at Junchuan town of Hubei Province, China were investigated.
Abstract: The objective of this study was to investigate the effects of short-term (less than 2 years) conservation managements [no-tillage (NT) and crop residue returning] on top soil (0–5 cm) microbial community composition and soil organic C (SOC) fractions under a rice-wheat rotation at Junchuan town of Hubei Province, China. Treatments were established following a split-plot design of a randomized complete block with tillage practices [conventional tillage (CT) and NT] as the main plot and residue returning level [no residue returning (0) and all residues returned to fields from the preceding crop (S, 2,146 kg C ha−1)] as the subplots. The four treatments were CT with or without residue returning (CT0 and CTS) and NT with or without residue returning (NT0 and NTS). The abundances of microbial groups [total FLFAs, fungal biomass, bacterial biomass, fungal biomass/bacterial biomass (F/B), monounsaturated fatty acids/saturated fatty acids (MUFA/STFA), and microbial stress] were determined by phospholipid fatty acid (PLFA) analysis of soil. The ratio of MUFA/STFA reflects aeration of soil and greater MUFA/STFA means better aeration condition of soil. Moreover, the microbial stress, the ratio of cy19:0 to 18:1ω7, was regarded as an indicator of physiological or nutritional stress of microbial community. PLFA profiles were dominated by the fatty acids iC15:0 (9.8 %), C16:0 (16.5 %), 10Me17:0 (9.9 %), and Cyc19:0 (8.3 %), together accounting for 44.6 % of the total PLFAs. Compared with CT, NT significantly increased microbial biomass C (MBC) by 20.0 % but did not affect concentrations of total organic C (TOC), dissolved organic C (DOC), easily oxidizable C (EOC), and SOC of aggregates. Residue returning significantly increased MBC by 18.3 % and SOC content of 2–1-mm aggregate by 9.4 %. NT significantly increased total PLFAs by 9.8 % and fungal biomass by 40.8 % but decreased MUFA/STFA by 15.5 %. Residue returning significantly enhanced total PLFAs, bacterial biomass, fungal biomass, F/B, and MUFA/STFA by 31.1, 36.0, 95.9, 42.5, and 58.8 %, respectively, but decreased microbial stress by 45.9 %. Multivariate analysis (redundancy analysis and partial correlation analysis) indicated that SOC of 2–1-mm aggregate was related to changes in the composition of soil microbial groups, suggesting that SOC of 2–1-mm aggregate was sensitive to changes in soil microbial community composition affected by short-term conservation management practices in our study.

110 citations


Journal ArticleDOI
TL;DR: Results show that AMF play an important role in mitigating drought impacts on soybean, but that mixtures of AMF isolates did not perform as well as the best single strain inoculum, excluding complementarity effects and suggesting selection effect of AMf on DS alleviation in soybean.
Abstract: It is well known that arbuscular mycorrhizal fungi (AMF) effects on plant growth largely depend on fungus identity. The objective of this study was to test whether three individual AMF isolates and their mixture mitigate drought stress (DS) differentially in soybean (Glycine max) genotype, predicting that under DS, the mixture of the AMF isolates would provide greater benefits to soybean plants than individual ones. In a greenhouse experiment, a drought-susceptible soybean genotype was inoculated with Septoglomus constrictum, Glomus sp., and Glomus aggregatum, known to be among the most abundant in agricultural and natural soils from central Argentina, and their mixture (Mx). Whereas under well-watered (WW) conditions, individual isolates and Mx treatment were similarly infective; under DS conditions, the Mx treatment showed lower rates of root colonization. Between WW and DS conditions, biomass was decreased in all treatments, although this effect was more marked in non-AM plants. Moreover, AMF strains improved water content and P and N concentrations. Under DS, the Mx treatment was unable to exceed the highest contents that were recorded by AMF isolates. However, under WW conditions, the Mx treatment showed a higher N content than individual isolates. Under both watering conditions, AM plants reduced oxidative damage evaluated as malondiadehyde and chlorophyll content and keep constant osmotic metabolites such as soluble sugars and proline content, without significant differences between AMF isolates and the Mx treatment. These results show that AMF play an important role in mitigating drought impacts on soybean, but that mixtures of AMF isolates did not perform as well as the best single strain inoculum, excluding complementarity effects and suggesting selection effect of AMF on DS alleviation in soybean.

105 citations


Journal ArticleDOI
TL;DR: Investigation of the diversity of bacterial communities associated with the spores of six AMF isolates found diverse bacterial community profiles unrelated with their taxonomic position suggesting that each AMF isolate recruits on its spores a different microbiota.
Abstract: Arbuscular mycorrhizal fungi (AMF) establish mutualistic symbioses with the roots of most food crops, playing a key role in soil fertility and plant nutrition and health. The beneficial activity of AMF may be positively affected by bacterial communities living associated with mycorrhizal roots, spores and extraradical hyphae. Here, we investigated the diversity of bacterial communities associated with the spores of six AMF isolates, belonging to different genera and species and maintained for several generations in pot cultures with the same host plant, under the same environmental conditions and with the same soil. The occurrence of large bacterial communities intimately associated with spores of the AMF isolates was revealed by PCR denaturing gradient gel electrophoresis (DGGE) analysis and sequencing of DGGE bands. Cluster and canonical correspondence analysis showed that the six AMF isolates displayed diverse bacterial community profiles unrelated with their taxonomic position, suggesting that each AMF isolate recruits on its spores a different microbiota. The 48 sequenced fragments were affiliated with Actinomycetales, Bacillales, Pseudomonadales, Burkholderiales, Rhizobiales and with Mollicutes-related endobacteria (Mre). For the first time, we report the occurrence of Mre in Funneliformis coronatum and Rhizophagus intraradices and sequences related to endobacteria of Mortierella elongata in F. coronatum and Funneliformis mosseae. The bacterial species identified are known to possess diverse and specific physiological characteristics and may play multifunctional roles affecting the differential performance of AMF isolates, in terms of infectivity and efficiency.

98 citations


Journal ArticleDOI
TL;DR: In this paper, the effects of biochar mineral nutrients, pH, and volatile matter (VM) on BNF in common beans (Phaseolus vulgaris L) were investigated.
Abstract: Studies document increases in biological nitrogen fixation (BNF) following applications of biochar. However, the underlying mechanisms for this response remain elusive. Greenhouse experiments were conducted to test the effects of biochar mineral nutrients, pH, and volatile matter (VM) on BNF in common beans (Phaseolus vulgaris L.). Biochars were produced from seven feedstocks pyrolyzed at either 350 or 550 °C. Biochars were treated with acid to reduce mineral nutrient contents, with acetone to remove acetone-soluble VM, with steam to reduce both the mineral and VM contents, or left untreated. The biochar additions at a rate of 15 t ha−1 resulted in an average 262 % increase in shoot biomass, 164 % increase in root biomass, 3575 % increase in nodule biomass, and a 2126 % increase in N derived from atmosphere (Ndfa) over the control. Simple mineral nutrients and soil acidity amelioration from the biochar were only to a minimal extent responsible for these increases (r 2 = 0.03; P = 0.0298, n = 201). Plant growth and Ndfa were significantly correlated with plant P uptake (r 2 = 0.22; P 0.05). Improved P nutrition resulted from 360 % greater mycorrhizal colonization with biochar additions. Removal of acetone-soluble VM increased plant growth and Ndfa, and VM extracted from the biochar produced at 350 °C reduced the growth of rhizobia in yeast extract mannitol agar (YMA) medium. In contrast, acetone-soluble VM extracted from seven biochars produced at 550 °C increased the growth of rhizobium in the YMA compared to an acetone-residue control, suggesting differential effects of VM forms on rhizobia.

92 citations


Journal ArticleDOI
TL;DR: In this paper, the effect of biochar type on plant performance and soil nitrogen (N) transformations in mesocosms representing an organic lettuce (Lactuca sativa) production system was investigated.
Abstract: We investigated the effect of biochar type on plant performance and soil nitrogen (N) transformations in mesocosms representing an organic lettuce (Lactuca sativa) production system. Five biochar materials were added to a silt loam soil: Douglas fir wood pyrolyzed at 410 °C (W410), Douglas fir wood pyrolyzed at 510 °C (W510), pine chip pyrolyzed at 550 °C (PC), hogwaste wood pyrolyzed between 600 and 700 °C (SWC), and walnut shell gasified at 900 °C (WS). Soil pH and cation exchange capacity were significantly increased by WS biochar only. Gross mineralization increased in response to biochar materials with high H/C ratio (i.e., W410, W510, and SWC), which can be favorable for organic farming systems challenged by insufficient N mineralization during plant growth. Net nitrification was increased by W510, PC, and WS without correlating with the abundance of ammonia oxidizing gene (amoA). Increases in N transformation rates did not translate into increases in plant productivity or leaf N content. WS biochar increased the abundance of amoA and nitrite reductase gene (nirK), while SWC biochar decreased the abundance of amoA and nitrous oxide gene (nosZ). Decreases in N2O emissions were only observed in soil amended with W510 for 3 days out of the 42-day growing season without affecting total cumulative N2O fluxes. This suggests that effects of biochar on decreasing N2O emissions may be transient, which compromise biochar’s potential to be used as a N2O mitigation strategy in organic systems. Overall, our results confirm that different biochar materials can distinctively affect soil properties and N turnover.

Journal ArticleDOI
TL;DR: In this paper, the authors evaluated the relationship between SOC accumulation rate, soil aggregation, microenvironment and microbial community composition using phospholipid fatty acid (PLFA) analysis.
Abstract: Repeated compost or inorganic fertilization may increase soil organic C (SOC) but how SOC accumulation relates to changes in soil aggregation, microenvironment and microbial community structure is unclear. Arable soils (Aquic Inceptisol) following a 20-year (1989–2009) application of inorganic fertilizer nitrogen (N), phosphorus (P) and potassium (K) (NPK), fertilizer NP (NP), fertilizer NK (NK), fertilizer PK (PK), compost (CM), half compost N plus half fertilizer N (HCM), and non-fertilization (Control) were collected to evaluate the relationship between SOC accumulation rate, soil aggregation, microenvironment and microbial community composition using phospholipid fatty acid (PLFA) analysis. Compared to the starting year, SOC content after 20 years under CM, HCM and NPK was significantly (P < 0.05) increased by 172 %, 107 % and 56 %, respectively, and by less than 50 % under NP, NK and PK. The mass proportion of macroaggregates was increased by 101–250 % under CM, but was not significantly affected by inorganic fertilizations, except PK. Compost and NPK significantly (P < 0.05) reduced the effective diffusion coefficient of oxygen primarily by increasing the proportion of pores <4 μm, and in contrast, increased the abundance of branched PLFAs and Gram-positive (G+) bacteria, resulting in the reduction of the ratio of monounsaturated/branched PLFAs (M/B) compared with Control. The mass proportion of macroaggregates was significantly (P < 0.01) and negatively correlated with the effective diffusion coefficient of oxygen; the latter was positively associated with M/B ratio. The SOC accumulation rate (z) had a significant interaction with the mass proportion of macroaggregates (x) and M/B ratio (y) (z = 0.514 + 4.345e x-15–0.149e y ). Our results suggested that SOC accumulation promoted the macroaggregation and reduced the effective diffusion coefficient of oxygen, causing changes in microhabitats and a shift in microbial community composition to more facultative and/or obligate anaerobes; such microbial community shifts favored accumulation of SOC in turn.

Journal ArticleDOI
TL;DR: The interaction between minerals and organic matter (OM) is a key to the turnover of OM in soils as mentioned in this paper, in particular, clay minerals, iron oxides and charcoal are considered as important constituents affecting the sequestration of carbon (C) and nitrogen (N).
Abstract: The interaction between minerals and organic matter (OM) is a key to the turnover of OM in soils. In particular, clay minerals, iron oxides and charcoal are considered as important constituents affecting the sequestration of carbon (C) and nitrogen (N). Here, we incubated pre-produced artificial soils (842 days) and a natural soil (Ap, Luvisol) with 13C- and 15N-labelled plant litter over 63 days to follow OM turnover and the formation of organo-mineral associations regarding different compositions (montmorillonite (MT), illite (IL), montmorillonite + charcoal (MT+CH), illite + ferrihydrite (IL+FH)). The microbial biomass, salt extractable organic C, the isotopic C and N composition in the bulk soil and the soil fractions (combined density and particle size fractionation) were determined. By comparison of the artificial soils with the natural soil, we were able to show that the produced soil-like systems have OM dynamics comparable to the natural soil. We found out that the decomposition of the added plant litter was affected by the type of clay mineral that formed the artificial soils, as the soil MT exhibited a slower mineralisation compared to IL, which was in line with a lower microbial biomass. Although a high specific surface area (SSA) provides a high sequestration capacity for C and N, smaller amounts were sequestered in the MT soil with a higher SSA compared to the soil IL. We suppose that a more intensive decomposition is associated with a higher microbial biomass and thus leads to higher amounts of microbial products sequestered in the clay-sized fraction. Charcoal and ferrihydrite had no additional effect in this experiment.

Journal ArticleDOI
TL;DR: In this article, the effects of lime and fly ash liming agents on the microbial community composition, enzyme activities involved in C, N, P, and S cycling and rice yields of acid sulfate soils were studied in a three-year field trial.
Abstract: The effects of calcium-magnesium phosphate, rock phosphate, lime, fly ash, and animal manure as liming agents on the microbial community composition, enzyme activities involved in C, N, P, and S cycling and rice yields of acid sulfate soils were studied in a three-year field trial. Significant increases in soil pH caused by five ameliorants, particularly lime and fly ash, were observed after 3 years. Both soil exchangeable Al3+ and H+ were significantly (P < 0.05) and negatively correlated with soil pH. Increased pH led to 61–102 % increase in rice yield after 2 and 3 years but not after 1 year. Soil phospholipid fatty acid (PLFA) profiles and enzyme activities were significantly changed after 3 years of application of the soil amendments. Enzyme activities increased along gradients of soil pH, indicating that the influences of inorganic or organic ameliorants on soil enzyme activities were mainly due to the effect on soil pH value. PLFA analysis showed that this pH effect played a more important role in shaping microbial community composition than specific effects of organic and inorganic amendments. All rice yield-associated enzymes and PLFA biomarkers (e.g., gram-negative bacteria and actinomycetes) were regulated by soil pH after 3 years. These results revealed that pH-induced changes in soil enzyme activity and microbial composition might be an important mechanism in alleviating acid stress in soil cropped to rice by various ameliorants.

Journal ArticleDOI
TL;DR: The hypothesis that plant genotype and fertilization conditions should be taken into account when searching for N-fixer inocula is supported.
Abstract: This research has investigated the effect of two genotypes of maize (Zea mays L.) on the number and diversity of diazotrophic bacteria under different N-fertilization rates. Cultivars NK940 and PAU871 were grown in soil:sand with 0, 40, and 80 kg N ha−1 added as NH4NO3 under controlled conditions for 60 days. The number of diazotrophic bacteria of rhizosphere (S), disinfected roots (R), and stems (T) was determined by most probable number (MPN) method. Diazotrophic bacteria were isolated by N-free media, confirmed by amplification of nifH gene fragments, characterized by amplified 16S rDNA restriction analysis (ARDRA) and (GTG)5 fingerprinting, and identified by partial 16S ribosomal DNA (rDNA) sequence analysis. The diversity of the diazotrophic community from S and R was determined by Terminal Restriction Fragment Length Polymorphism (T-RFLP) analysis considering the nifH gene. Maize genotype had a marked effect on the number and diversity of endophytic communities, the NK940 community being more abundant and diverse than that of PAU871. Additionally, N-fertilization increased the number and diversity of diazotrophs in endophytic communities but not in rhizosphere samples. One hundred and six diazotrophs were isolated from S, R, and T samples. Pseudomonas and Enterobacter were the dominant and ubiquitous genera isolated and detected by culture-independent method. T-RFLP showed that the N-fixing populations of the rhizosphere of both cultivars were more diverse than those of inside roots. Principal component analysis (PCA) separated the samples by cultivar and demonstrated a more marked effect of N-fertilization on the NK940 diazotrophic community than on PAU871. These results support the hypothesis that plant genotype and fertilization conditions should be taken into account when searching for N-fixer inocula.

Journal ArticleDOI
TL;DR: In this article, the contribution of crop straw to microbial organic C (MBC) was quantified and the effect of different soil fertility levels on the distribution of straw-derived soil organic C pools was evaluated.
Abstract: Microorganisms mediate the decomposition of straw residue in soil, but how soil fertility levels affect microbial incorporation of straw C remains unclear in many ecosystems. The objectives of this study were to quantify the contribution of straw C to microbial organic C (MBC), and to evaluate the effect of different soil fertility levels on the distribution of straw-derived soil organic C (SOC) pools. An in situ incubation was set up with soils amended with or without 13C-labeled maize straw. Across fertility treatments, straw C retained in soil decreased, on average, from 84 % after 30 days (June 5, 2011) to 30 % after 365 days (May 5, 2012). Over the entire incubation, 2–5 % of straw C was incorporated to MBC. At the high and medium fertility levels, MBC contained, on average, 58 % of straw C and 42 % of native SOC, respectively, whereas more than 75 % of MBC was derived from straw C at the low fertility level. Total MBC was lower in soil at the low fertility level compared with soils at the high and medium fertility levels. These results suggest that in low fertility soils, the addition of crop straw significantly promoted the activity and growth of soil microorganisms and provided a potential positive feedback to soil fertility.

Journal ArticleDOI
TL;DR: At the site under study biopores as pathways for rapid root growth into deeper soil layers allow roots to re-enter and explore the subsoil, cereals cultivated in rotation with taprooted crops can draw benefit from enhanced uptake of water and nutrients from deeper soil layer during early growth stages.
Abstract: Taprooting crop species are capable of creating soil biopores (>2 mm in diameter) in the subsoil due to their large root size and deep-rooting habit. The aim of this study was to quantify root growth dynamics of wheat in the subsoil during its complete growth season as affected by crop sequence. Temporal observation on root length (km m−2) of wheat inside and outside of biopores at four growth stages (tillering, booting, anthesis, and milk) was conducted by using the profile wall method under the two crop sequence treatments involving two precrops, viz., chicory and tall fescue. Frequency of biopore presence measured on vertical profile walls depended on the choice of precrops in which chicory precrop resulted in higher frequency (2.3 %) compared with tall fescue (1.5 %). Root length of wheat measured inside biopores was significantly higher when grown after chicory (0.024 km m−2) in comparison to tall fescue (0.006 km m−2). On average, root length outside biopores after growing chicory was 45.9 % higher than tall fescue until the stage of anthesis. We conclude that at the site under study biopores as pathways for rapid root growth into deeper soil layers allow roots to re-enter and explore the subsoil. Thus, cereals cultivated in rotation with taprooted crops can draw benefit from enhanced uptake of water and nutrients from deeper soil layers during early growth stages. Model simulations with various abiotic and biotic factors will be helpful to reveal the direct evidence of biopore-root-shoot relationship in the future.

Journal ArticleDOI
TL;DR: In this paper, the authors studied 1 and 2 years after biochar, phosphorus (P), and biochar+P additions to the soil of a north temperate, mixed-deciduous, P-limited forest in Central Ontario, Canada.
Abstract: Soil microbial biomass, activity, and community composition were studied 1 and 2 years after biochar, phosphorus (P), and biochar + P additions to the soil of a north temperate, mixed-deciduous, P-limited forest in Central Ontario, Canada. Biochar was pyrolyzed on site from sugar maple and white spruce sawdust at ca. 400 °C, and P was added as triple superphosphate. Biochar additions of 5 t ha−1 (approximately 0.4 to 1 kg P ha−1) had minor effects on bacterial and fungal community composition, fungi/bacteria ratios, microbial biomass, and microbial C mineralization, with significant changes only being detected in the organic layer for additions of maple biochar. In contrast, additions of 200 kg P ha−1 did alter soil chemical properties and reduced both microbial biomass and fungi/bacteria ratios. We conclude that biochar addition at 5 t ha−1 is neither beneficial nor toxic to the soil microbes in a northern hardwood forest on acidic soils, suggesting that biochar amendments can be used to sequester C without adversely affecting the soil microbial community.

Journal ArticleDOI
TL;DR: It is suggested that seasonal and environmental factors play a major role on AMF abundance and diversity than short-term agronomic practices, including AMF inoculation.
Abstract: Arbuscular mycorrhizal fungal (AMF) communities are fundamental in organic cropping systems where they provide essential agro-ecosystem services, improving soil fertility and sustaining crop production. They are affected by agronomic practices, but still, scanty information is available about the role of specific crops, crop rotations and the use of winter cover crops on the AMF community compositions at the field sites. A field experiment was conducted to elucidate the role of diversified cover crops and AMF inoculation on AMF diversity in organic tomato. Tomato, pre-inoculated at nursery with two AMF isolates, was grown following four cover crop treatments: Indian mustard, hairy vetch, a mixture of seven species and a fallow. Tomato root colonization at flowering was more affected by AMF pre-transplant inoculation than by the cover crop treatments. An enormous species richness was found by morphological spore identification: 58 AMF species belonging to 14 genera, with 46 and 53 species retrieved at the end of cover crop cycle and at tomato harvest, respectively. At both sampling times, AMF spore abundance was highest in hairy vetch, but after tomato harvest, AMF species richness and diversity were lower in hairy vetch than in the cover crop mixture and in the mustard treatments. A higher AMF diversity was found at tomato harvest, compared with the end of the cover crop cycle, independent of the cover crop and pre-transplant AMF inoculation. Our findings suggest that seasonal and environmental factors play a major role on AMF abundance and diversity than short-term agronomic practices, including AMF inoculation. The huge AMF diversity is explained by the field history and the Mediterranean environment, where species characteristic of temperate and sub-tropical climates co-occur.

Journal ArticleDOI
TL;DR: Zhang et al. as discussed by the authors investigated how fertilization affects soil organic C (SOC) sequestration and soil C fractions in a rice-barley system of eastern China after 23-year repeated organic and chemical fertilizer amendments.
Abstract: Fertilizer application can potentially change soil organic C (SOC) sequestration of croplands. However, how fertilization affects SOC sequestration and soil C fractions has not been sufficiently investigated. Here, we studied this issue in a rice–barley system of eastern China after 23-year repeated organic and chemical fertilizer amendments. The fertilization treatments were as follows: unfertilized control (CK), pig manure (M), chemical fertilizer NPK (NPK), and pig manure combined with NPK (MNPK). Our results showed that M, NPK, and MNPK significantly increased 25, 13, and 30 % of SOC content as compared with CK. Compared with CK, the three fertilizations, especially manure addition, significantly increased the content of SOC fractions such as microbial biomass C, dissolved organic C, labile organic C, and particulate organic C. Compared with the initial SOC stock at 0–20-cm depth (41.2 Mg C ha−1), M, NPK, and MNPK increased 11, 1, and 16 % of SOC storage, respectively, whereas CK decreased 9 % of SOC pool. The SOC sequestration was positively correlated with the cumulative C input (root residue-C + manure-C) (SOC sequestration = 0.21 × C input − 5.67, R 2 = 0.88, P < 0.001). This linear relationship suggested that (i) the soil had not reached a SOC saturation, (ii) the conversion rate from input-C to SOC was 21 %, and (iii) a C input threshold of 1.17 Mg C ha−1 year−1 was needed for maintaining the initial SOC level. Therefore, manure application is recommended for promoting SOC sequestration in the rice–barley cropping system of eastern China.

Journal ArticleDOI
Fucui Li1, Zhaohui Wang1, Jian Dai1, Qiang Li1, Xiang Wang, Cheng Xue1, Hui Liu1, Gang He1 
TL;DR: The application of inorganic N fertilizer in combination with appropriate crop residues may be an effective approach to improve the long-term fertilizer N use efficiency, soil quality, and crop yield in wheat–summer fallow rotation systems in dryland.
Abstract: Returning crop residues to soil is an effective approach for sustaining organic matter concentrations and increasing nutrient availability in soils. A 2-year micro-plot field experiment was conducted in dryland to determine the green manure, straw, and fertilizer nitrogen (N)-15 uptake by wheat, their residual N in soil and losses; the effect of straw application on the fate of N from green manure and vice versa was also determined, as well as the effect of crop residue additions on the fate of fertilizer N. All the micro-plots were treated with the same amount of 15N-labeled or unlabeled fertilizer. The green manure N uptake by wheat, residual N, and N loss were 22.4, 51.7, and 25.9 % of the total added green manure N over the 2-year experiment. Straw addition significantly decreased the green manure residual soil N but increased the cumulative losses. The straw N taken up by wheat, residual N in soil, and N loss were 8.3, 31.0, and 60.7 %, respectively. Green manure addition significantly decreased the straw N taken up by wheat, increased the residual soil N, and reduced the N loss. Furthermore, the fertilizer N taken up by wheat, residual N in soil, and N loss were 32.4, 32.3, and 35.2 %, respectively. Crop residue additions significantly increased the uptake of fertilizer N by wheat in the second year. The application of inorganic N fertilizer in combination with appropriate crop residues may be an effective approach to improve the long-term fertilizer N use efficiency, soil quality, and crop yield in wheat–summer fallow rotation systems in dryland.

Journal ArticleDOI
TL;DR: X-ray tomography was used to obtain 3D information on the burrowing behaviour of six very common anecic and endogeic earthworms and observed a linear relationship between burrow length and the water infiltration rate.
Abstract: Earthworm burrow systems are generally described based on postulated behaviours associated with the three eco- logical types. In this study, we used X-ray tomography to obtain 3D information on the burrowing behaviour of six very common anecic (Aporrectodea nocturna and Lumbricus terrestris) and endogeic (Aporrectodea rosea, Allolobophora chlorotica, Aporrectodea caliginosa, Aporrectodea icterica) earthworm species, introduced into repacked soil cores for 6 weeks. A simple water infiltration test, the Beerkan method, was also used to assess some functional properties of these burrow systems. Endogeic worms make larger burrow sys- tems, which are more highly branched, less continuous and of smaller diameter, than those of anecic worms. Among the anecic species, L. terrestris burrow systems are shorter (9.2 vs 21.2 m) with a higher number (14.5 vs 23.5) of less branched burrows (12.2 vs 20.2 branches m �1 ), which are also wider (7.78 vs 5.16 mm) than those of A. nocturna .I n comparison, the burrow systems made by endogeic species appeared sim- ilar to each other. However, A. rosea burrows were short and narrow, whereas A. icterica had a longer burrow system (15.7 m), more intense bioturbation intensity (refilled macropores or soil lateral compaction around them) and thus a greater number of burrows. Regarding water infiltration, anecic burrow systems were far more efficient due to open burrows linking the top and bottom of the cores. For endogeic species, we observed a linear relationship between burrow length and the water infiltration rate (R 2 =0.49, p<0.01). Overall, the three main characteristics significantly influenc- ing water infiltration were burrow length, burrow number and bioturbation volume. This last characteristic highlighted the effect of burrow refilling by casts.

Journal ArticleDOI
TL;DR: In this paper, the influence of different trap solutions and collection times on the quali-and quantitative root exudation pattern of white lupin (Lupinus albus L.) grown under phosphorus (P) and iron (Fe) deficiency was assessed.
Abstract: White lupin is very often used as a model plant for root exudation studies due to its capability to release huge amounts of organic acids and flavonoids. The complex nature of these organic compounds makes not only their analytical determination difficult but also their extraction from soil samples. For these reasons simplified approaches, as hydroponic-based systems are widely used to study the root exudation. Therefore, the composition of a trap solution is crucial to limit artefacts causing over/underestimation of exudation rates and/or a biased molecular composition of the collected compounds. The present study was aimed at assessing the influence of different trap solutions and collection times on the quali- and quantitative root exudation pattern of white lupin (Lupinus albus L.) grown under phosphorus (P) and iron (Fe) deficiency. Our results suggest that, in works aimed at studying root exudation processes, water is the most effective trap solution to collect the exudates like organic acids and flavonoids, especially in short time (e.g. 2 h). For longer times, low concentrations of Ca could be helpful to limit osmotic stress and possible passive leakage and/or diffusion. The use of bacteriostatic compounds as NaN3 and Micropur bias the results, due to interferences either with the metabolism or inhibition of the exudation processes, especially in the case of flavonoids such as quercetin. Also, the use of a pH buffer solution like 2-(N-morpholino)ethanesulfonic acid (MES) should be avoided for its undesired interferences with the release.

Journal ArticleDOI
TL;DR: In this paper, the effects of urea and nitrification inhibitors (NIs) on inorganic N concentrations and N2O emissions were evaluated in three aerobic incubation experiments to establish the relationship between nitrite concentration and N 2O emission by adding different amounts of nitrite to soil, and identify the contributions of abiotic processes to N 2 O production from nitrite by sterilization.
Abstract: It has been widely demonstrated—both in the field and the laboratory—that N fertilization stimulates peaks in nitrous oxide (N2O) emissions in agricultural soils. However, the mechanisms responsible for this phenomenon remain unclear. In this study, three aerobic incubation experiments were designed to: (1) evaluate the effects of urea and nitrification inhibitors (NIs) on inorganic N concentrations and N2O emissions; (2) establish the relationship between nitrite concentration and N2O emission by adding different amounts of nitrite to soil, and identify the contributions of abiotic processes to N2O production from nitrite by sterilization; and (3) explore the underlying reasons for nitrite accumulation by using 15N tracer methods. Compared with NI treatments, substantial nitrite accumulated in the UREA treatment, mainly attributed to the inhibitory effects of high ammonium from urea hydrolysis on transformation of 15N-nitrite to 15N-nitrate. N2O emission from soil was related to soil nitrite concentration, according to the Michaelis–Menten relationship (R 2 = 0.998; P < 0.01). No significant N2O emission was observed in sterilized soil, indicating that N2O production was a microbial process with the probable dominance of nitrifier denitrification (ND). In conclusion, our results suggest that ammonium fertilizer stimulates nitrite accumulation by inhibiting nitrite transformation to nitrate, thus resulting in an increase in N2O emissions, while NIs reduce N2O emissions by suppressing nitrite formation.

Journal ArticleDOI
TL;DR: In this paper, the authors traced C derived from corn silage hydrochar (δ13C of −13 ‰) added to coarse and fine textured soils over two cropping seasons.
Abstract: Soil amendment with hydrochar produced by hydrothermal carbonization of biomass is suggested as a simple, cheap, and effective method for increasing soil C. We traced C derived from corn silage hydrochar (δ13C of −13 ‰) added to “coarse” and “fine” textured soils (δ13C of −27 ‰ for native soil C (SOC)) over two cropping seasons. Respiration rates increased in both soils (p < 0.001) following hydrochar addition, and most of this extra respiration was derived from hydrochar C. Dissolved losses accounted for ~5 % of added hydrochar C (p < 0.001). After 1 year, 33 ± 8 % of the added hydrochar C was lost from both soils. Decomposition rates for the roughly two thirds of hydrochar that remained were very low, with half-life for less estimated at 19 years. In addition, hydrochar-amended soils preserved 15 ± 4 % more native SOC compared to controls (negative priming). Hydrochar negatively affected plant height (p < 0.01) and biomass (p < 0.05) in the first but not the second crop grown on both soils. Our results confirm previous laboratory studies showing that initially, hydrochar decomposes rapidly and limits plant growth. However, the negative priming effect and persistence of added hydrochar C after 1 year highlight its soil C sequestration potential, at least on decadal timescales.

Journal ArticleDOI
TL;DR: In this article, the authors refer to the original definition of the ecosystem given by Tansley and apply it to the soil viewed as a multi-scale assemblage of ecological systems.
Abstract: Can soil be considered as just a component of terrestrial ecosystems and agro-ecosystems or is it an ecosystem in itself? The present piece of opinion suggests that we should refer to the original definition of the ecosystem given by Tansley and apply it to the soil viewed as a multi-scale assemblage of ecological systems.

Journal ArticleDOI
Jiahui Shao1, Zhihui Xu1, Nan Zhang1, Qirong Shen1, Ruifu Zhang1 
TL;DR: The rhizospheric strain B. amyloliquefaciens SQR9 may be used as a plant-growth-promoting agent to increase crop yield and can be attributed to multiple factors, including production of phytohormones, volatile compounds, and extracellular enzymes.
Abstract: Bacillus amyloliquefaciens SQR9, isolated from the rhizosphere of cucumber, can control Fusarium wilt of cucumber and directly stimulate plant growth. To evaluate its potential agricultural use, the plant growth promotion of B. amyloliquefaciens SQR9 was evaluated, and the relative mechanisms, especially the production of the phytohormone indole-3-acetic acid (IAA), were investigated. The related plant-growth-promoting factors were genetically and chemically analyzed, and a mutant library was constructed for selecting strains with different IAA production. B. amyloliquefaciens SQR9 showed a growth-promoting activity in greenhouse experiments. Plant-growth-promoting factors like extracellular phytase, volatile components including acetoin, 2,3-butanediol, and phytohormone IAA were detected in B. amyloliquefaciens SQR9 cultures grown under laboratory conditions. Three IAA production mutant strains showed variation in plant-growth-promoting effect. IAA production in B. amyloliquefaciens SQR9 was related to its plant-growth-promoting effect, but IAA alone could not account for the overall observed plant-growth-promoting effect. The promoted plant growth by the rhizospheric strain B. amyloliquefaciens SQR9 can be attributed to multiple factors, including production of phytohormones, volatile compounds, and extracellular enzymes. Therefore, the strain B. amyloliquefaciens SQR9 may be used as a plant-growth-promoting agent to increase crop yield.

Journal ArticleDOI
TL;DR: Bio-inoculation of yerba mate seedlings with native PGPR increases the yield of this crop in nursery and could represent a promising sustainable strategy to improve yerBA mate growth in low-fertility soils.
Abstract: In this study, the role of native plant growth-promoting rhizobacteria (PGPR) as bio-inoculants was assessed as an alternative to ameliorate Ilex paraguariensis St. Hill. growth in nursery comparing poorer (soil) versus richer (compost) substrates. Twelve rhizospheric strains isolated from yerba mate plantations were evaluated in vitro for their potential as PGPRs. Three isolates, identified as Kosakonia radicincitans YD4, Rhizobium pusense YP3, and Pseudomonas putida YP2, were selected on the basis of their N2 fixation activity, IAA-like compound and siderophore production, and phosphate solubilization. A highly significant positive effect of bio-inoculation with the native isolates was observed in 5-month-old seedlings cultivated in soil. The highest increase was observed in seedlings inoculated with K. radicincitans YD4 with an increase of 183 % in the dry shoot weight and a 30 % increase in shoot N content. In contrast, in compost, no increment in the dry weight was observed; however, an increase in content in some macronutrients in shoots was observed. Remarkably, when plant biomass was compared between soil and compost, seedlings inoculated with K. radicincitans YD4 in soil produced the highest yields, even though higher yields could be expected in compost due to the richness of this substrate. In conclusion, bio-inoculation of yerba mate seedlings with native PGPR increases the yield of this crop in nursery and could represent a promising sustainable strategy to improve yerba mate growth in low-fertility soils.

Journal ArticleDOI
TL;DR: Results suggest that pathogenic fungal build-up and a reduction in the abundance of beneficial rhizobacteria in the rhizosphere contribute to changes in soil suppressiveness to soil-borne pathogens in monocropped soils, resulting in an aggravated level of soil sickness.
Abstract: Cotton yield and quality have been severely compromised by soil sickness throughout the primary cotton-growing regions of China. The aim of this study was to gain insight into the role of rhizosphere microbial community in governing soil sickness of cotton. Plant growth, disease resistance, root exudates, and the composition of the rhizosphere microbial community of cotton were analyzed in two different (4- and 15-year) monocropped soils and in a fallow agricultural soil (control). The monocropped soils significantly influenced cotton growth and root exudates and reduced soil suppressiveness to Fusarium wilt in bioassay experiments. Additionally, pyrosequencing of the whole internal transcribed spacers (ITS1 and ITS2) and 16S rRNA gene amplicons demonstrated clear variations in the microbial composition of cotton rhizosphere between monocropped rhizosphere soils and control soil. Specifically, monocropped soils were characterized by an increase in the abundance of fungal pathogens, including Fusarium oxysporum f. sp. vasinfectum and Verticillium dahliae, relative to the rhizosphere of control soil. Some plant-beneficial and disease-suppressive bacterial taxa, including Xanthomonadaceae, Comamonadaceae, Oxalobacteraceae, and Opitutaceae, were associated with healthy cotton. A significant correlation existed between the presence of certain amino acids (e.g., glutamic acid and alanine) and the above identified taxa, indicating that some constituents in root exudates influenced the microbial compositions of the cotton rhizosphere to manage the disease status of plant in monocropped soils. Collectively, these results suggest that pathogenic fungal build-up and a reduction in the abundance of beneficial rhizobacteria in the rhizosphere contribute to changes in soil suppressiveness to soil-borne pathogens in monocropped soils, resulting in an aggravated level of soil sickness.

Journal ArticleDOI
TL;DR: Six barley cultivars widely differing for cadmium (Cd) tolerance, partitioning, and translocation were analyzed and indicated that the different capacity of each cultivar to maintain GSH homeostasis under Cd stress may strongly affect PC accumulation and, thus, Cd tolerance and translocated.
Abstract: Six barley cultivars widely differing for cadmium (Cd) tolerance, partitioning, and translocation were analyzed in relation to their thiol metabolism. Results indicated that Cd tolerance was not clearly related to the total amount of Cd absorbed by plants, resulting instead closely dependent on the capacity of the cultivars to trap the metal into the roots. Such behaviors suggested the existence of root mechanisms preserving shoots from Cd-induced oxidative damages, as indicated by the analysis of thiobarbituric acid-reactive substances—diagnostic indicators of oxidative stress—whose increases in the shoots were negatively related to Cd root retention and tolerance. Cd exposure differentially affected glutathione (GSH) and phytochelatin (PC) levels in the tissues of each barley cultivar. The capacity to produce PCs appeared as a specific characteristic of each barley cultivar, since it did not depend on Cd concentration in the roots and resulted negatively related to the concentration of the metal in the shoots, indicating the existence of a cultivar-specific interference of Cd on GSH biosynthesis, as confirmed by the existence of close positive linear relationships between the effect of Cd on GSH levels and PC accumulation in both roots and shoots. The six barley cultivars also differed for their capacity to load Cd ions into the xylem, which was negatively related to PC content in the roots. Taken as a whole, these data indicated that the different capacity of each cultivar to maintain GSH homeostasis under Cd stress may strongly affect PC accumulation and, thus, Cd tolerance and translocation.