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The user has requested enhancement of the downloaded file. BURLEIGH DODDS SERIES IN AGRICULTURAL SCIENCE Achieving sustainable crop nutrition Edited by Professor Zed Rengel University of Western Australia, Australia E-CHAPTER FROM THIS BOOK The effect of soil organic matter on plant mineral nutrition O. Urrutia, J. Erro, M. Fuentes, M. Olaetxea and M. Garnica, University of Navarra, Spain; R. Baigorri, TIMAC AGRO, UK; A. M. Zamarreño, M. Movila and D. De Hita, University of Navarra, Spain; and J. M. Garcia-Mina, University of Navarra, Spain and Centre Mondial De L’Innovation Roullier, France 1 Introduction 2 The main mechanisms involved in the beneficial action of humic substances on plant mineral nutrition: the complexing and biochemical pathways 3 A possible signalling crosstalk between the biochemical and complexing pathways 4 Conclusion 5 Acknowledgements 6 Where to look for further information 7 References 1 Introduction The functional relationships between soil fertility and the content of natural organic matter in soil are well known (Chen et al., 2004a; Magdoff and Weil, 2004). One of the main components of soil organic matter (SOM) is soil humus, which results from the abiotic and biotic transformation of fresh organic matter in soil (Chen et al., 2004a; Stevenson, 1994). Soil humus, in fact, is a very complex organic system including simple biomolecules as well as highly complex and transformed biomolecules that are normally known as humic substances (HS) (Stevenson, 1994; Wershaw, 1993; Piccolo, 2002; Baigorri et al., 2007). From an operational viewpoint, HS are fractionated in the laboratory into three main fractions: (i) the humic acids (HA) that are soluble at basic pH but not at acidic pH, (ii) the fulvic acids (FA) that are soluble at both acidic and basic pH and (iii) the humin that is insoluble in water regardless of pH (Stevenson, 1994). The HA fraction may be further separated to grey HA and brown HA taking advantage of their different solubility at neutral pH and high ionic strength (Stevenson, 1994; Baigorri et al., 2007). http://dx.doi.org/10.19103/AS.2019.0062.14 © Burleigh Dodds Science Publishing Limited, 2020. All rights reserved. Chapter taken from: Rengel, Z. (ed.), Achieving sustainable crop nutrition, Burleigh Dodds Science Publishing, Cambridge, UK, 2020, (ISBN: 978 1 78676 312 9; www.bdspublishing.com) 2 The effect of soil organic matter on plant mineral nutrition Although the chemical nature and structural features of HS are the object of intense discussion in the literature (Lehmann and Kleber, 2015; Olaetxea et al., 2018), recent studies have demonstrated that these organic molecules have specific structural features that are not present in well-defined biomolecules such as proteins, microbial metabolites, polysaccharides, lignin or cellulose (Cao and Schmidt-Rorh, 2018). These distinctive structural features appear to be related to specific distributions of aromatic moieties in large aliphatic ones in the complex molecular aggregates (Perminova et al., 2018). Molecular aggregation provides HS with some new chemical properties such as amphiphilicity that influences their ability to interact with inorganic and organic molecules, as well as with root surfaces (Olaetxea et al., 2018) (Fig. 1). The emergence of new properties associated with molecular aggregation allows us to consider HS as a family of natural supramolecules (Piccolo, 2002). In fact, the supramolecular and macromolecular characters of HS are coexisting in solution. Thus, grey HA is mainly macromolecular, whereas brown HA and, principally, FA are supramolecular (Baigorri et al., 2007; Garcia-Mina, 2007). Many studies have reported the capacity of HS to improve the growth of plants cultivated in soils as well as in inert substrates and hydroponics (Chen and Aviad, 1990; Chen et al., 2004a; Rose et al., 2014; Canellas et al., 2015). In general, the various effects caused by HS in plants are divided into two main classes: the indirect effects resulting from the interaction of HS with the main components of the soil and rhizosphere and the direct effects resulting from the interaction of HS with cell membranes at root surface (Chen and Aviad, 1990; Chen et al., 2004a; Olaetxea et al., 2018). Both types of HS-mediated effects affect plant mineral nutrition. The indirect effects of HS include an increase in the fraction of bioavailable nutrients in the rhizosphere, whereas Figure 1 A structural model of leonardite humic acid proposed from the C13-NMR, FTIR, dynamic light scattering and elemental analysis data (the primary structure has been optimized using the Hyperchem 8.0 software). © Burleigh Dodds Science Publishing Limited, 2020. All rights reserved. The effect of soil organic matter on plant mineral nutrition 3 the direct effects are related to a high efficiency in nutrient uptake by roots and further utilization within the plant. In this chapter we discuss these effects of HS on plant mineral nutrition as well as possible signalling pathways involved in their regulation and interactions. 2 The main mechanisms involved in the beneficial action of humic substances on plant mineral nutrition: the complexing and biochemical pathways 2.1 The indirect effects of humic substances on plant mineral nutrition The capacity of HS, both HA and FA, to interact with metals in soils and waters has been well established by many studies (Stevenson, 1994; Chen and Aviad, 1990; Chen et al., 2004a; Senesi, 1992; Tipping, 2002). This capacity of HS lies in the presence of certain functional groups in the HS structure. These functional groups can contain oxygen (O) (e.g. carboxylic, hydroxyl, phenolic and carbonyl), nitrogen (N) (e.g. amide, amine) or sulphur (S) (e.g. sulfhydryl) (Stevenson, 1994; Senesi, 1992; Tipping, 2002) (Fig. 2). Through these functional groups, HS react with metals, forming stable complexes in soil solution and soil interphases (Stevenson, 1994; Senesi, 1992; Tipping, 2002) (Fig. 3a). Two main types of HS-metal interactions can be defined depending on whether the interaction influences the water solubility and bioavailability of cations – for example, some micronutrients such as iron (Fe), copper (Cu), zinc (Zn) or manganese (Mn), or anions (mainly phosphate). In the case of micronutrient availability, the direct binding of the metal to the binding sites in HA has most relevance, whereas for macronutrient availability this interaction also involves the binding of the anion to the HS-binding sites through the metal bridges (Chen et al., 2004a; Urrutia et al., 2013, 2014). 2.1.1 Humic substances – metal complexation affecting micronutrient availability Many studies have demonstrated that soil pH and soil mineral composition affect the availability of the main micronutrients with metallic character, mainly Fe, Cu, Mn and Zn (Mortvedt et al., 1991). Thus, alkaline and calcareous soils favour micronutrient precipitation in the form of hydroxides that are rapidly transformed into stable oxides (Mortvedt et al., 1991). This precipitation is associated with a decrease in the availability of these micronutrients to plants and microorganisms that, in turn, causes nutritional deficiencies that are behind significant reductions in crop yield and fruit quality (Mortvedt et al., 1991). In this context, many studies have reported the beneficial action of SOM, and principally of HS, on © Burleigh Dodds Science Publishing Limited, 2020. All rights reserved. 4 The effect of soil organic matter on plant mineral nutrition Figure 2 Main functional groups present in humic substances that may act as binding sites for metal complexation. Figure 3 (a) Fe complexation by a salycilic type-binding site in humic substances (HS); (b) Phosphate binding in a salycilic type-binding site in HS through an Fe bridge. (hydrogen atoms in white; carbon atoms in grey; oxygen atoms in red; iron atoms in purple; phosphorus atoms in yellow.) © Burleigh Dodds Science Publishing Limited, 2020. All rights reserved. The effect of soil organic matter on plant mineral nutrition 5 micronutrient availability resulting from their capacity to form stable and watersoluble metal complexes (Chen and Aviad, 1990; Chen et al., 2004a). In fact, the major fraction of these micronutrients that is present in the soil solution of alkaline and calcareous soils is in the form of stable complexes with the dissolved organic matter (DOM)-humic fractions (Geering et al., 1969; Mortvedt et al., 1991). The role of HS as enhancers of micronutrient availability for plants has great relevance in case of Fe. Many studies have demonstrated that HS are directly involved in the availability of Fe in alkaline and calcareous soils, as probably the most important growth-promoting action of HS, principally in soils with low SOM (Chen et al., 2004a,b). Some studies suggest that this might also be the case for other micronutrients such as Zn and Cu (Chen et al., 2004a,b; GarciaMina et al., 2004). It is noteworthy that the maximum stability and water solubility of these HS-metal complexes correspond to a pH interval 7–10 that is associated with the minimum water solubility of the free metals (Tipping, 2002; Garcia-Mina et al., 2004; Garcia-Mina, 2006). Likewise, acidic pH values that are associated with high (in some cases toxic) micronutrient concentrations in soil solutions are linked to low HS-metal stability and water solubility (Garcia-Mina et al., 2004; Garcia-Mina, 2006). There exists certain specificity in the functional groups involved in the complexation of each metal. Thus, carboxylic groups in aliphatic domains appear to be the major ligands for Fe complexation, whereas phenols at alkaline pH and amines at acidic pH are likely to be the major binding sites for Cu complexation (Fuentes et al., 2013). Studies involving HS-metal complexes and plants growing in soil or hydroponics under micronutrient deficiency have demonstrated the capacity of plant roots to hydrolyse the HS-metal bonds and take up micronutrients (Chen et al., 2004a,b; Garcia-Mina et al., 2004; Urrutia et al., 2014). This process appears to involve local acidification of root surface as well as the possible release of complexing and/or reducing agents as root exudates (Chen et al., 2004a,b; Garcia-Mina et al., 2004; Urrutia et al., 2014). Efficiency of natural HS-metal complexes to alleviate micronutrient deficiency has promoted development of similar metal-complexing compounds in laboratory and in large-scale production as potential correctors of micronutrient deficiency in crops (Garcia-Mina et al., 2004 and references therein). 2.1.2 Humic substances – metal complexation affecting macronutrient availability Phosphorus (P) availability is very low in alkaline/calcareous as well as acidic soils (Urrutia et al., 2014 and references therein). In calcareous soils © Burleigh Dodds Science Publishing Limited, 2020. All rights reserved. 6 The effect of soil organic matter on plant mineral nutrition phosphate tends to precipitate as calcium phosphates, whereas in acidic soils phosphate availability is decreased by the formation of Fe and aluminium (Al) phosphates as well as the adsorption on clay minerals (Urrutia et al., 2014). In this context, several studies have shown that, as in the case of metallic micronutrients, the presence of humified organic matter in soil increases phosphate solubility in soil solution and, thereby, P availability (Urrutia et al., 2014). Among different mechanisms that may explain the beneficial effects of SOM on P availability, the potential formation of stable compounds containing both HS and phosphate appears to play a relevant role (Gerke, 2010; Urrutia et al., 2014). A number of studies have shown that the capacity of HS to form stable complexes with metals can also influence availability of some macronutrients, mainly P. This is because HS can complex P by the formation of metal bridges between the negatively charged functional groups in HS and the phosphate anion (Gerke, 2010; Urrutia et al., 2013, 2014) (Fig. 3b). Several studies have demonstrated that this HS-metal-P (phosphate) type of complex has stability similar to that of HS-metal complexes (Guardado et al., 2005, 2007, 2008; Urrutia et al., 2013, 2014). However, various plant species were shown to hydrolyse these HS-metal-P complexes at the root surface and take up both the metal and phosphate (Urrutia et al., 2013). In fact, fertilizers that contain these P-humic complexes have proved to be highly effective in providing available P to plants growing in alkaline/calcareous as well as acidic soils (Erro et al., 2007, 2009, 2012). Similarly, the formation of stable humicmetal complexes with sulphate might also improve plant uptake of S (Baigorri et al., 2013). HS may also improve N and K plant uptake (Olaetxea et al., 2018). As discussed in the following sections, such improvements appear to be related to the direct HS effects on enhancing nutrient uptake by roots. In fact, the chemical interaction between HS functional groups and K or ammonium is mainly ionic and quite weak. Likewise, there is no experimental evidence showing stable chemical interactions between HS and nitrate (Stevenson, 1994). 2.1.3 Conclusions These results clearly show that HS may benefit plant mineral nutrition by increasing the pool of available nutrients present in soil, particularly in the rhizosphere, via complexation. The chemical activity of HS relies on the presence of specific functional groups distributed throughout their structure, allowing formation of stable metal complexes with variable water solubility depending on pH and metal:HS ratio. © Burleigh Dodds Science Publishing Limited, 2020. All rights reserved. The effect of soil organic matter on plant mineral nutrition 7 2.2 The direct effects of humic substances on plant mineral nutrition In addition to the previously discussed indirect effects of HS influencing nutrient availability in soils, a number of studies have reported the capacity of HS to also influence nutrient root uptake mechanisms as well as nutrient metabolism in plants (Nardi et al., 2002; Olaetxea et al., 2018). These direct effects arising from the interaction of HS with cells at the root surface result in the HS-dependent regulation of the biochemical and molecular networks associated with root nutrient uptake at the three levels: 1 The root plasma membrane (PM) H+-ATPase activity, 2 Specific root nutrient transporters, and 3 Major enzymes involved in nutrient utilization within plants. As in the case of the complexing action of HS, several studies have shown that the physiological effects associated with the direct effects of HS are greatly influenced by the structural features of HS (Garcia et al., 2016). 2.2.1 The effects of humic substances on the root PM-ATPase at the transcriptional and enzyme-activity levels Proton transport is directly involved in the generation of membrane potential gradients and, therefore, in the regulation of many processes associated with the transport of minerals and organic solutes. Proton transport is governed by plasma membrane H+-ATPase activity, with the energy needed for setting up the gradients provided by ATP hydrolysis (Falhof et al., 2016). In this framework, it becomes clear that those compounds that stimulate PM H+ATPase activity at the root surface may promote transport of many ions into plant tissues. A number of studies have demonstrated the capacity of HA extracted from diverse organic substrates (leonardite, peat and vermicompost) to significantly increase root PM H+-ATPase activity (Pinton et al., 1999; Canellas et al., 2002; Mora et al., 2010). This effect was associated with stimulation of some processes related to the development of both roots and shoots, such as lateral root proliferation and shoot growth (Zandonadi et al., 2007, 2010; Mora et al., 2010). Likewise, the HA-mediated increase in the root PM H+-ATPase activity was also linked to the increase in root uptake of some nutrients such as nitrate (Pinton et al., 1999) or Fe (Aguirre et al., 2009). In addition, HA caused an increase in the root-to-shoot translocation of practically all nutrients, likely linked to the HA capacity to promote root-to-shoot cytokinin transport (Mora et al., 2010; Olaetxea et al., unpublished results). © Burleigh Dodds Science Publishing Limited, 2020. All rights reserved. 8 The effect of soil organic matter on plant mineral nutrition The effects of HS on root PM H+-ATPase activity were accompanied by significant up-regulation of the genes encoding some isoforms of the root PM H+-ATPase in cucumber (Aguirre et al., 2009). It was noteworthy that the isoform transcriptionally up-regulated by HA (Cs-HA2) was different from that up-regulated by Fe deficiency (Cs-HA1) (Aguirre et al., 2009). Another study in maize also showed that HA extracted from vermicompost may up-regulate the expression of the ZmHA2 gene (Quaggiotti et al., 2004). Similarly, HA extracted from leonardite up-regulated the genes coding for other ATPase isoforms in cucumber in addition to Cs-HA2, such as the Cs-HA4, Cs-HA8 and Cs-HA9 (Olaetxea et al., unpublished results). It is likely that root uptake of other major nutrients is also enhanced by a HS-influenced increase in root PM H+-ATPase activity, particularly in case of K and sulphate as well as Mg and Ca (Marschner, 2012). 2.2.2 The effects of humic substances on root nutrient transporters In addition to the previously discussed action of HS on root PM H+-ATPase activity, a number of studies have demonstrated the capacity of HA of diverse origin to regulate the expression of genes encoding major nutrient transporters in roots (Olaetxea et al., 2018 and references therein). Regarding Fe, many studies have reported the capacity of HA extracted from leonardite to increase the expression of the gene encoding an Fe(II) transporter, IRT1, in the roots of cucumber plants growing with no limitation of Fe availability (Aguirre et al., 2009). Other studies have also observed an increase in the IRT1 expression in the roots of rapeseed plants treated with HA extracted from black peat (Jannin et al., 2012). These effects caused by HA of diverse origin were associated with significant increases in Fe root uptake and further translocation from roots to shoots (Aguirre et al., 2009; Jannin et al., 2012). In wheat (strategy II plant species, Marschner, 2012), the root application of leonardite HA under Fe-limiting conditions was associated with an increase in the root release of phytosiderophores compared with non-treated Fe-deficient plants, with this effect being linked to a significant increase in the remobilization of Fe within the plant (Garnica et al., unpublished results). In addition, the application of HA extracted from black peat to rapeseed roots increased the expression of genes encoding COMT2 and NRAMP3, two transporters involved in transport of Cu, Zn and Mn within the plant (Billard et al., 2014). Hence, HS improve micronutrient uptake not only by enhancing their availability in the rhizosphere through complexation, but also by improving the functioning of nutrient transporters in the global plant nutrient-uptake network system. Regarding macronutrients, a number of studies have reported a significant increase in the expression of some nitrate transporters in diverse plant species (Olaetxea et al., 2018 and references therein). Quaggiotti et al. (2004) observed © Burleigh Dodds Science Publishing Limited, 2020. All rights reserved. The effect of soil organic matter on plant mineral nutrition 9 that HA extracted from the earthworm faeces up-regulated the expression of gene coding for a specific nitrate transporter (ZmNRT2.1) in leaves, but not roots, of maize. Peat-derived HA applied to rapeseed roots was associated with up-regulation of both BnNRT1.1 and BnNRT2.1 in roots and an increase in nitrate uptake (Jannin et al., 2012). More recently, Tavares et al. (2017) reported the capacity of HA extracted from vermicompost to up-regulate OsNRT2.12.2 and OsNAR2.1 as well as some ATPase isoforms in rice. In maize treated with water-extracted peat HA, Zanin et al. (2018) also observed significant up-regulation of these nitrate transporters. Similar results to those previously discussed in relation to nitrate were also observed in the case of sulphate in rapeseed plants treated with HA extracted from peat (Jannin et al., 2012). Root application of HA up-regulated the expression of sulphate transporters in roots (BnSulftr1.1 and 1.2) as well as another S transporter involved in sulphate sequestration in shoot vacuoles, resulting in increased sulphate uptake (Jannin et al., 2012). The results regarding phosphate are less clear. Vermicompost HA up-regulated the expression of a phosphate transporter in roots (LPT2) of tomato plants growing in P-replete medium; however, this effect was not observed in tomato growing under P deficiency (Jindo et al., 2016). Regarding K root uptake, a recent study showed that an HA extracted from terrestrial organic sediments prevented degradation of the high-affinity K+ transporter 1 (HKT1) in Arabidopsis, thus improving plant growth under salinity (Khaleda et al., 2017). 2.2.3 Effects on the activity of major enzymes involved in nutrient utilization in plants Several microarray studies have reported that HS have major effects of the expression of a large number of genes, and activity of corresponding enzymes, involved in practically all aspects of plant metabolism, including nutrient use (Trevisan et al., 2011; Jannin et al., 2012). Significantly increased nitrate reductase activity was reported in both roots and shoots of rapeseed plants treated with peat-derived HA (Jannin et al., 2012) and of cucumber plants treated with HA extracted from leonardite (Mora et al., 2010). Other studies have reported significant increases in the main enzymes involved in ammonium metabolism such as glutamine synthetase and glutamate synthase (Conselvan et al., 2017). These effects on N metabolism were also reflected in changes in the protein patterns in HA-treated plants (Carletti et al., 2008). Leonardite-derived HA increased the activity of phosphoenolpyruvate carboxylase (PEP-carboxylase, an enzyme directly involved in phosphate availability in the TCA cycle), and up-regulated the gene encoding this enzyme in cucumber (Lemenager et al., unpublished results). © Burleigh Dodds Science Publishing Limited, 2020. All rights reserved. 10 The effect of soil organic matter on plant mineral nutrition Humic acids induced significant variations in the enzymatic network involved in carbon metabolism (including glycolysis and Krebs cycle) as well as phenolic synthesis (Conselvan et al., 2017). 2.2.4 Conclusions The findings discussed previously show that HS act as efficient enhancers of nutrient uptake by roots and further utilization in plants. These effects result from the interaction of HS with the root-cell plasma membrane and could be denoted as the biochemical pathway by which HS improve plant mineral nutrition. As discussed in the next section, it is plausible that the biochemical pathway is interconnected at a molecular level with the complexing pathway occurring in the rhizosphere. 3 A possible signalling crosstalk between the biochemical and complexing pathways A number of studies have shown that the plant-growth promoting action of HS involves the participation of several inter-related signalling pathways (Olaetxea et al., 2018 and references therein). An increase in shoot growth caused by leonardite-derived HA was expressed through the IAA- and nitric oxide (NO)dependent signalling pathways (Mora et al., 2014), with root ABA also having an important role in this process (Olaetxea et al., 2015). Finally, both root PM H+-ATPase and cytokinins play a crucial role in the regulation of the HA activity in shoot growth (Olaetxea et al., unpublished results), whereas both root PM H+ATPase and root ABA have a vital role in the HA action in root growth (Olaetxea et al., unpublished results). It is noteworthy that these two signalling pathways are regulated, although not exclusively, by IAA (Zandonadi et al., 2010; Mora et al., 2014). It is likely that one or more signalling pathways activated by HS may be involved in the regulation of the effects of HS on nutrient transporters and enzyme activities. A plausible hypothesis is that HS act through the IAA-H+ATPase pathway because this pathway is associated with the regulation of, and energy supply to, most nutrient transports (Falhof et al., 2016). However, new experiments involving IAA- or H+-ATPase-defective mutants, and/or IAA-H+ATPase inhibitors are needed in order to explore this hypothesis. On the other hand, several studies have revealed a role of some nutrient transporters influenced by HS as the sensors of nutrient concentrations in the root medium (Ho and Tsay, 2010). The examples are CHL1/NRT1.1-2.1 for nitrate (Ho et al., 2009; Vert and Chory, 2009; Gojon et al., 2011) and IRT1 for Fe (II) (Dubeaux et al., 2018), which are known as transceptors. Other studies indicated that NRT2.1 may affect IAA-dependent processes such as © Burleigh Dodds Science Publishing Limited, 2020. All rights reserved. The effect of soil organic matter on plant mineral nutrition 11 lateral root development (Little et al., 2005). Hence, it is plausible that these transceptors might play a role in regulating the crosstalk between the two pathways (complexing and biochemical) involved in beneficial activity of HS in plant mineral nutrition. For example, in plants growing under Fe-limiting conditions, as in calcareous soils, IRT1 (Fe(II) transporter) may act as a sensor of Fe concentration in soil solution, with Fe under these soil conditions being in the form of soluble Fe-HA complexes (the complexing pathway), and trigger the all-root responses to Fe-limiting conditions that include the processes involved in the biochemical pathway. In this way, the complexing and the biochemical pathways will be closely related to each other through IRT1. Nevertheless, new specifically designed experiments are needed in order to check this hypothesis. 4 Conclusions The mechanisms involved in the beneficial action of soil humus, and more specifically HS, on plant mineral nutrition are multiple, complex and likely interconnected. We have denoted two main routes: one related to the reaction between HS and nutrients in soil (complexing pathway) and another linked to the effects of HS on the molecular and biochemical network involved in nutrient uptake by roots and further utilization in plants (biochemical pathway). The two modes of action of HS are directly linked to the structural properties and functional features of HS. It is plausible that the two modes of action could be the two sides of a single and complex mechanism. In this framework, the relative importance of each pathway is determined by the concentration of HS in soil solution; interestingly, the concentration needed to cause direct effects in plants (150–300 mg L-1) is higher than that necessary to increase micronutrient availability (10–50 mg L-1) (Chen and Aviad, 1990). Thus, in soils with very low concentration of HS in the soil solution (but with most of metallic micronutrients in the form of soluble humic complexes) the complexing pathway will be more important than the biochemical pathway. Conversely, in plants with relatively high HS concentration in the rhizosphere the biochemical pathway may also be important. The transceptor role of some nutrient transporters influenced by HS opens up a possibility of a single general pathway combining the complexing and biochemical pathways. 5 Acknowledgements We would like to thank the Regional Government of Navarra, the Government of Spain, the University of Navarra Research Foundation as well as the Roullier Group for their support and funding. © Burleigh Dodds Science Publishing Limited, 2020. All rights reserved. 12 The effect of soil organic matter on plant mineral nutrition 6 Where to look for further information Further information about the role of HS in plant mineral nutrition and plant growth can be found in the web page of the International Society of Humic substances (IHSS) (www.humic-substances.org/). In this site a collection of selected articles as well as the most relevant published books about humic substances’ structural features, physico-chemical features and biological activity can be found. Also the main contacts in different countries can be also found there. 7 References Aguirre, E., Leménager, D., Bacaicoa, E., Fuentes, M., Baigorri, R., Zamarreño, A. M. and García-Mina, J. M. 2009. The root application of a purified leonardite humic acid modifies the transcriptional regulation of the main physiological root responses to Fe deficiency in Fe-sufficient cucumber plants. Plant Physiol. Biochem. 47(3), 215–23. doi:10.1016/j.plaphy.2008.11.013. 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