MINI REVIEW article
From Lab to Field: Role of Humic Substances Under Open-Field and Greenhouse Conditions as Biostimulant and Biocontrol Agent
- 1Agrosystems Research, Wageningen University and Research, Wageningen, Netherlands
- 2Núcleo de Desenvolvimento de Insumos Biológicos para a Agricultura (NUDIBA), Universidade Estadual do Norte Fluminense Darcy Ribeiro, UENF, Rio de Janeiro, Brazil
- 3Department of Soil and Water Conservation and Organic Waste Management, Centro de Edafolog a y Biología Aplicada del Segura (CEBAS)-Consejo Superior de Investigaciones Cient ficas (CSIC), Campus Universitario de Espinardo, Murcia, Spain
The demand for biostimulants has been growing at an annual rate of 10 and 12.4% in Europe and Northern America, respectively. The beneficial effects of humic substances (HS) as biostimulants of plant growth have been well-known since the 1980s, and they can be supportive to a circular economy if they are extracted from different renewable resources of organic matter including harvest residues, wastewater, sewage sludge, and manure. This paper presents an overview of the scientific outputs on application methods of HS in different conditions. Firstly, the functionality of HS in the primary and secondary metabolism under stressed and non-stressed cropping conditions is discussed along with crop protection against pathogens. Secondly, the advantages and limitations of five different types of HS application under open-fields and greenhouse conditions are described. Key factors, such as the chemical structure of HS, application method, optimal rate, and field circumstances, play a crucial role in enhancing plant growth by HS treatment as a biostimulant. If we can get a better grip on these factors, HS has the potential to become a part of circular agriculture.
The function and application of biostimulants and biopesticides have garnered considerable interest due to their potential as environmentally sustainable resources for agricultural production. A number of national and international projects on biostimulant material have been launched in the framework of the circular economy by extracting the beneficial material from waste materials across different sectors of agriculture, livestock, water infrastructure, mining, and energy (Xu and Geelen, 2018). Notably, the projects BIO-FERTIL (Poland), BIOFECTOR (Germany), and HUMIC-XL (Netherlands) have highlighted the potential use of humic substances (HS) from waste material for plant growth, which can be a component of a local circular economy. To provide scientific evidences of the potential use of biostimulants, several reviews have been published recently (Calvo et al., 2014; du Jardin, 2015; Van Oosten et al., 2017; Abbott et al., 2018; Bulgari et al., 2019; Juárez-Maldonado et al., 2019; Pylak et al., 2019). In general, HS, seaweed extracts, beneficial microorganisms, and chitosan and protein hydrolases are listed in the mentioned review papers. While the chitosan and protein hydrolases are becoming popular as a biostimulant in the last decade (Drobek et al., 2019), utilization of HS, composed of humic (HA) and fulvic acid (FA), has been recognized as a long-run product since the 1980s (Calvo et al., 2014). The underlying function of HS as biological activation for plant growth has been strongly related to the chemical composition (e.g., functional groups), hydrophobicity, and flexible conformational structure of HS (Muscolo et al., 2013; Canellas and Olivares, 2017). Whereas a large number of scientific publications are related to the impact of HS in hydroponic assays and under growth chamber conditions (Nardi et al., 2000, 2018; Russell et al., 2006), reports on its potentiality in the field and under greenhouse conditions are less explored, mainly due to the variety of underlying factors in crop fields, including weather variability and climate fluctuations, soil type, and field management. For all these reasons, review reports on the practical application of HS in fields are scarce (Rose et al., 2014; Canellas et al., 2015b). The main focus of the present work is to (1) describe the mechanisms of the HS effect on plant growth, and (2) to illustrate the HS utilization under open-field and greenhouse conditions.
Key Benefits of HS on Plant Growth
One of the major impacts of HS on plant growth is the reinforcement in nutrient uptake and the elongation of the lateral root growth, often recognized as “auxin-like effect,” which is a result of the induction of ATPase activity in the plasma membrane (Maggioni et al., 1987; Nardi et al., 1991; Pinton et al., 1992; Canellas et al., 2002; Quaggiotti et al., 2004; Zandonadi et al., 2007). The underlying mechanisms are generating a wider electrochemical gradient by ATPase induction and accelerating the nutrient uptake rate, which can also be confirmed by the overexpression of the transporter genes (Jindo et al., 2016; Zanin et al., 2018; Nunes et al., 2019). The availability of micronutrients such as iron can be improved with HSs, not only by chelation but also by promoting the root capability to uptake nutrients from the soil solution (Aguirre et al., 2009; Zanin et al., 2019).
Understanding the underlying mechanisms of plant response is a noteworthy keystone for the HS use in the field, and the first step would be a better understanding of the effect of HS on carbon and nitrogen cycles, which is related to primary metabolism (Canellas and Olivares, 2014; Olk et al., 2018; Canellas et al., 2019). HS also interferes with secondary metabolism by altering gene expression and changing the content of chemical compounds in plant cells, such as those related to the Krebs cycle, metabolism of nitrate and phosphorus, glycolysis, and photosynthesis (Roomi et al., 2018; Lotfi et al., 2018).
Historically, from the 1980s until the end of the 1990s, studies on the effect of HS on photosynthesis and ATP production were the major topics of research. A critical view of these works can be found in the previous papers of Nardi et al. (2002, 2009). Trevisan et al. (2011) found a high level of transcription of genes involved in primary metabolism in Arabidopsis thaliana and supported previous studies about the physiological effects of HS on plant metabolic pathways. Nardi et al. (2007) evaluated the impact of different HS on the enzymatic activities involved in glycolytic and respiratory processes of maize seedlings including glucokinase, phosphoglucose isomerase, PPi-dependent phosphofructokinase, and pyruvate kinase, as well as the activity of citrate synthase, malate dehydrogenase, and isocitrate NADP+ -isocitrate dehydrogenase. In the proteomic analysis conducted by Nunes et al. (2019), differences were detected in the maize seedling root proteins related to energy metabolism, cytoskeleton, cellular transport, conformation and degradation of proteins, and DNA replication. Thirty-four proteins were significantly more abundant in the seedlings treated with HA, whereas only nine proteins were abundant in the control. The main effect of HA was protective, mainly associated with increased expression of 2-cys peroxidase, putative VHS/GAT, and glutathione proteins (Nunes et al., 2019).
The transcriptome and proteome are more abundantly reported than metabolomics studies. The plant metabolome is the entirety of the small molecules present in the plant and can be regarded as the ultimate expression of its genotype in response to environmental changes (Fiehn, 2002). Aguiar et al. (2018) observed that the application of HA on sugarcane significantly decreased the concentration of 15 metabolites, which generally included amino acids. HA increased the levels of 40 compounds, which are associated with the stress response (shikimic, caffeic, hydroxycinnamic acids, putrescine, behenic acid, quinoline xylulose, galactose, lactose proline, oxyproline, and valeric acid), and this is aligned with up-regulation of the protein involved in redox homeostasis (Roomi et al., 2018).
Plant secondary metabolism produces a large number of specialized compounds that do not directly aid in the growth and development of plants but are required for the plant to survive in its environment and under biotic and abiotic stress. Salinity and drought are the most frequent stresses studied in fields and under greenhouse conditions (Ali et al., 2020). Several reports have been published on the impact of HS on the growth of pepper, common beans, rice, tomato, corn, sorghum, and cucumber under these stress conditions (Demir et al., 1999; García et al., 2012; Berbara and García, 2014; Rose et al., 2014; Prado et al., 2016; Van Oosten et al., 2017; Bulgari et al., 2019; Pinos et al., 2019; Ali et al., 2020). One of the underlying mechanisms of the impact of the HS is the interaction with auxin, jasmonic acid and abscisic acid by phytohormonal regulation in the root, which are well-known plant hormones for the stress of drought and salinity (De Hita et al., 2019; Ali et al., 2020). Another example is the synthesis of flavonoids, which are involved in the interception of ultraviolet (UV) as an adaptive mechanism preventing UV in plant physiology (Hollósy, 2002). HA could induce the activity of the first enzyme in the phenylpropanoid pathway at the level of gene expression, similarly to other studies in which phenylpropanoid synthesis has been enhanced by fungal elicitors and hormones (Schiavon et al., 2010; Lewis et al., 2011).
The increase in phenolic compounds is another typical plant response to HA treatment (Ertani et al., 2011). During the progress of the domestication of cultivated plants over 10,000 years, the bitter and astringent taste from phenolic compounds, which often produced in the phenylpropanoid pathway of the secondary metabolism, has been gradually eliminated, resulting in the reduction of the natural plant protection against stress (Wink, 1988). The foliar application of HA improves this ancient mechanism reducing plant infection (Olivares et al., 2015) as well as enhancing plant protection (Hernandez et al., 2014).
Finally, HS is involved in the enhancement of plant protection against infestation. Joshi et al. (2014) present the list of pathogens and pests controlled through vermicompost application, highlighting that the main chemical components of the vermicompost belong to HS. There are four approaches by which HS can contribute to the plant defense mechanisms under field and greenhouse conditions: (1) enhancing the soil microbial activities that play as biological control agents, such as Trichoderma (McLean et al., 2012; Motta and Santana, 2013; Mohamadi et al., 2017); (2) direct interaction with plant pathogen (e.g., Nematodes, Late blight) (Zaller, 2006; Seenivasan and Senthilnathan, 2018; D’Addabbo et al., 2019; Liu et al., 2019); (3) physical protection for beneficial microbes, such as UV protection (Bitton et al., 1972; Muela et al., 2008; Kaiser et al., 2019); (4) enhancing plant antioxidant defense system against pathogen by modulating chemical compounds (e.g., phenols) and enzymes (e.g., phenylalanine ammonia-lyase) (Kesba and El-Beltagi, 2012; Olivares et al., 2015).
Mode of Application in Fields
The functions of HS for the enhancement of plant growth widely differ depending on the application mode, plant stage, and its rate, which will be discussed in the subsequent sections. Basically, there exist five application types of HS in the field (Erro et al., 2016; Ekin, 2019).
Direct Application in Soil (Liquid Status)
Researches and farmers adopt the direct use of HSs as an aqueous suspension. The effect of the direct application of liquid status has been demonstrated on the growth of different crops such as Lettuce (Lactuva sativa) and Grape rootstocks (Vitis vinifera L.) (Supplementary Table S1). Comparative advantages of liquid formulation include the possibility to combine with other inputs such as chemical fertilizer or beneficial microorganisms and adaptability to agricultural machinery for the implementation. Application time, depending on the plant development stage, must be considered.
Direct Application in Soil (Solid Status)
The solid-state application of HSs has been less explored for implementation in the field when compared with liquid formulations. The main agricultural applications of HSs in the form of powder or granules are soil amendments and organo-mineral fertilizers that require the highest dose per plot (Supplementary Table S1). The solid application brings a problem of uniform distribution of aqueous dispersion after dissolution on rhizosphere, gradient concentration, and re-sedimentation of HA on soil solution. Despite the difficulty of obtaining uniform HS aqueous suspension at the optimal doses, different rates of solid HS application had shown a direct positive effect on plant stimulation or soil physicochemical properties (Supplementary Table S1). Powder HA applied to soil at a rate of 75 g m–2 increased yield of thyme (Thymus vulgaris L.) and quality of essential oil (Noroozisharaf and Kaviani, 2018). In the same study, the highest dose of HA powder (100 g m–2) improved nutrient content in leaves via positive modulation of nutrient transport through the chelation and stimulation of microbial activity by HS interaction. Undoubtedly, solid forms as powder or granules will be suitable in the future since the transport operation can be economically prohibitive for liquid HSs. However, a high volume of HS products is required for large-scale farming. Future research on the technology of on-farm solubilization of solid forms as stable final products will be demanded.
Since the 1940s and 1950s, scientific research on the beneficial impact of foliar application has been explored (Tanou et al., 2017). There exist two theories to explain how exogenous inputs via foliar application are delivered to plant cell tissue, once they reached leaf surface: (1) transfer into leaf tissues via transcuticular penetration (Smilkova et al., 2019); or (2) penetration through leaf stomata (Tejada et al., 2016). Many authors report that micronutrient contents are increased by HS rather than macronutrient in field level (Fernández-Escobar et al., 1996; Çelik et al., 2011; Fatma et al., 2015; Balmori et al., 2019). After foliar treatment, nutritional parameters of polyphenol content and antioxidant activity to determine the quality of fruit are improved (Tarantino et al., 2018). In practice, liquid compost extracts, fully enriched with HS, represent a cost-effective tool to conduct foliar application (Zandonadi et al., 2013; Berbara and García, 2014). A wide range of plants have been tested with HS application under open-field conditions, such as garlic (Balmori et al., 2019), common beans (Kaya et al., 2005; Souri and Aslani, 2018), wheat (Zhang et al., 2016; Ahmad et al., 2018; Bezuglova et al., 2019), fenugreek (Ibrahim, 2019), tomato (Olivares et al., 2017), asparagus (Tejada and Gonzalez, 2003), maize (Canellas et al., 2015a) and citrus tree (Hameed et al., 2018). Foliar application is frequently reported in calcareous soil conditions where nutrient uptake, especially iron, is limited due to precipitation (Çelik et al., 2011; Souri and Aslani, 2018; Bezuglova et al., 2019). Foliar spray application is limited to suitable climate conditions, since high temperature and windy and rainy days are not recommended. High application rates provoke leaf burning as water evaporates and salts remain on the leaves, especially at high temperature (Fageria et al., 2009). The developing stage has to be considered since foliar application cannot be conducted after flowering in rice production, which could cause spikelet discoloration. Crop responses to foliar application are unlikely positive when there is nutrient deficiency in the soil (Fageria et al., 2009). Taking all together, the impact of foliar-applied HS is less consistent than those observed when applied on the root, where HS is exposed to a more stable condition (De Hita et al., 2019).
Fertigation is extensively expanding over the world, especially in semi-arid and arid regions where water scarcity is an issue (Fallahi et al., 2017). García-Gaytán et al. (2018) widely describe the potential of different biostimulant materials used in fertigation. After the concentration of HS in rhizosphere increases by the irrigation, two contributions of HS to plant growth are presumably proposed: (1) straightening out soil fertility, which makes nutrient more available; (2) directly reaching out plant cell walls on the root surface so that plant can take up nutrients (Olaetxea et al., 2018). Regarding agronomic outcome in practice, Suman et al. (2016, 2017) showed the impact of the combined application of chemical fertilizer and HA in fertigation on productivity on capsicum and tomato under open-field conditions, concluding that HA could replace up to 20% of fertilizer. Selladurai and Purakayastha (2016) used a similar combination of liquid fertilizer by using the pedal-operated sprayer in soil in the open field, and they improved N, P, and K use efficiencies by 16.4, 9.3, and 18.3%, respectively. Water use also can be saved by the humic application (Selim and Mosa, 2012; Alenazi et al., 2016). The mode of fertigation has to be adjusted based on the type of crop. Selim et al. (2009) highlighted that subsurface drip irrigation method has a highly significant effect on potato tuber yield rather than surface drip irrigation, due to maintenance of optimum soil moisture content in the root zone in an Egyptian sandy soil. However, no effect was found in banana seedling with the drip irrigation with HS in tropical soil (de Melo et al., 2016), implying that crop and soil type have to be taken into account. A multiple-option of HS application, combining the use of solid HS at pre-sowing moment prior to fertigation with HS, can be useful to mitigate adverse environmental conditions (Smoleñ et al., 2017), or the use of wastewater for fertigation with HS incorporated into soil for saving water resources (Masciandaro et al., 2014).
A limited number of works are reported on the seedling with the immersion method under field and greenhouse condition (Bettoni et al., 2016a, b; Gemin et al., 2019). This method is commonly used in hydroponic and growth chamber conditions (Supplementary Table S1).
Benefits and Limitations of Hs Application in the Field
Proper implementation of HS in field conditions is an essential point for experiment design. Several works report a comparative study of different applications (Supplementary Table S1). Waqas et al. (2014) compared three application modes (foliar spray, soil application, and immersion) for mung bean. They concluded that no significant differences were observed across different applications. A similar result was reported by Karakurt et al. (2009) on pepper comparing between foliar spray and soil application. In contrast, other reports showed that foliar spray performed higher yield than soil application in tomato (Yildirim, 2007), maize (Tejada et al., 2016), almond (Saa et al., 2015), and sugarcane (Da Silva et al., 2017). An ideal implementation would be combined applications rather than a single application method, which was demonstrated in Bettoni et al. (2016b) with higher nutritional quality and yield of onion.
It is noteworthy that the positive effect of HS application on plant growth is not always guaranteed. The points of concern about the HS application are listed in Figure 1. In particular, the chemical structure of HS, optimum application rate, and the mode of use play a crucial role in performing a visible outcome on the ground. At first, finding out an optimal dosage is an essential process, and this is changeable with application mode and plant type. Some specific plants such as lettuce (L. sativa) from Asteraceae family and Arabdopsis thaliana from Brassicacea family are more sensitive to the change in the concentration of HS and application mode (Rodda et al., 2006; Dobbss et al., 2007; Hernandez et al., 2013). Secondary, the type of HS is a vital point, which is related to the chemical structure and molecular size of HS. The interaction between the chemical composition of HSs and bioactivity was studied (Canellas et al., 2009; Aguiar et al., 2013; Martinez-Balmori et al., 2014) and the importance of hydrophobic/hydrophilic ratio is a key factor as a suitable indicator to predict bioactivity based on their chemical properties. This ratio is prominently high in HA rather than FA due to the enrichment of the aromatic carbon group. Also, similar or even better crop responses have been achieved by HSs derived from compost rather than from leonardite, peat, or other pedogenic stable organic matter reservoirs (Ayuso et al., 1996). Another factor is the chemical variation due to different extraction techniques and nutrient enrichment processes (Hartz and Bottoms, 2010). In line with this study, Chen et al. (2004) concluded that soil application of commercial humic products at typical rates (2 to 3 kg ha–1) is ineffective in promoting significant agronomical response to different crops under an open-field condition.
Figure 1. Advantages and limitations of humic substance application under open-fields and greenhouse conditions.
Furthermore, Chen et al. (2004) highlighted that the recommended dose for commercial HS product is at least 10 times smaller than required to stimulate plant growth under laboratory and greenhouse assays (75 mg L–1, equivalent to 50 kg ha–1). Regarding soil types, Pylak et al. (2019) report that HSs are not particularly effective in reducing the solubility of heavy metals in acidic soils. Using commercial HA products in combination with liquid fertilizers, Hartz and Bottoms (2010) mentioned that a positive crop response was found only in soil with low organic matter content. Also, suitable application time is a concerned issue. While the use of HS at the early developing stage usually enhances the root elongation, sugar content, grain weight, and fruit size increase at a late vegetative stage (Canellas et al., 2015b).
HS application originally from wastes as a biostimulant for plant growth is a beneficial and eco-friendly approach, and it fits into the concept of circular economy focusing on the conversion to a new resource. Plant anatomical and biochemical changes in the root system by HS are the main factors responsible for increased nutrient uptake, although the increase in the nutrient availability through chelation is another HS contribution to plant growth. The hydrophobicity/hydrophilic ratio is a useful indicator to understand the chemical structure of HS and to estimate the effect on plant growth. Although different dose ranges of HS application in field and laboratory condition are suitable, it is recommendable to conduct a preliminary test to find an optimum rate considering crop type, soil properties, and application mode.
All authors contributed to the study conception, design, data collection, analyses, and manuscript preparation. KJ, FO, DM, LC, wrote the article. KJ, FO, MS-M, CK, and LC supervised and completed the writing. All authors read and approved the final manuscript.
KJ wishes to acknowledge financial support (3710473400-1). The authors FO, DM, and LC were supported by Fundação Carlos Chagas Filho de Amparo á Pesquisa do Estado do Rio de Janeiro (FAPERJ), Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES); Conselho Nacional de Desenvolvimento de Pesquisa e Tecnologia (CNPq), Newton Foundation and FINEP Pluricana Project.
Conflict of Interest
The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.
We acknowledge support of the publication fee by the CSIC Open Access Publication Support Initiative through its Unit of Information Resources for Research (URICI).
The Supplementary Material for this article can be found online at: https://www.frontiersin.org/articles/10.3389/fpls.2020.00426/full#supplementary-material
TABLE S1 | Effect of humic substance with different application modes on plant growth under different experimental conditions: Field trial (FD); Growth chamber (GC); Greenhouse (GH) Hydroponic (HP).
Abbott, L. K., Macdonald, L. M., Wong, M. T. F., Webb, M. J., Jenkins, S. N., and Farrell, M. (2018). Potential roles of biological amendments for profitable grain production – A review. Agric. Ecosyst. Environ. 256, 34–50. doi: 10.1016/j.agee.2017.12.021
Abdel-monaim, M. F., Ismail, M. E., and Morsy, K. M. (2011). Induction of systemic resistance of benzothiadiazole and humic acid in soybean plants against fusarium wilt disease. Mycobiology 39, 290–298. doi: 10.5941/MYCO.2011.39.4.290
Aguiar, N. O., Medici, L. O., Olivares, F. L., Dobbss, L. B., Torres-Netto, A., and Silva, S. F. (2016). Metabolic profile and antioxidant responses during drought stress recovery in sugarcane treated with humic acids and endophytic diazotrophic bacteria. Ann. Appl. Biol. 168, 203–213. doi: 10.1111/aab.12256
Aguiar, N. O., Novotny, E. H., Oliveira, A. L., Rumjanek, V. M., Olivares, F. L., and Canellas, L. P. (2013). Prediction of humic acids bioactivity using spectroscopy and multivariate analysis. J. Geochem. Explor. 129, 95–102. doi: 10.1016/j.gexplo.2012.10.005
Aguiar, N. O., Olivares, F. L., Novotny, E. H., and Canellas, L. P. (2018). Changes in metabolic profiling of sugarcane leaves induced by endophytic diazotrophic bacteria and humic acids. PeerJ 2018, 1–28. doi: 10.7717/peerj.5445
Aguirre, E., Diane, L., Eva, B., Marta, F., Roberto, B., and Zamarreño, A. 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, 215–223. doi: 10.1016/j.plaphy.2008.11.013
Ahmad, T., Khan, R., and Nawaz Khattak, T. (2018). Effect of humic acid and fulvic acid based liquid and foliar fertilizers on the yield of wheat crop. J. Plant Nutr. 41, 2438–2445. doi: 10.1080/01904167.2018.1527932
Ahmed, A. H., Darwish, E., Hamoda, S., and Alobaidy, M. (2013). Effect of putrescine and humic acid on growth, yield and chemical composition of cotton plants grown under saline soil conditions. Environ. Sci. 13, 479–497. doi: 10.5829/idosi.aejaes.2013.13.04.1965
Alenazi, M., Wahb-Allah, M. A., Abdel-Razzak, H. S., Ibrahim, A. A., and Alsadon, A. (2016). Water regimes and humic acid application influences potato growth, yield, tuber quality and water use efficiency. Am. J. Potato Res. 93, 463–473. doi: 10.1007/s12230-016-9523-9527
Alessa, O., Najla, S., and Murshed, R. (2017). Improvement of yield and quality of two Spinacia oleracea L. varieties by using different fertilizing approaches. Physiol. Mol. Biol. Plants 23, 693–702. doi: 10.1007/s12298-017-0453-458
Ali, A. Y. A., Ibrahim, M. E. H., Zhou, G., Nimir, N. E. A., Jiao, X., Zhu, G., et al. (2020). Exogenous jasmonic acid and humic acid increased salinity tolerance of sorghum. Agron. J 1–16. doi: 10.1002/agj2.20072
Ayuso, M., Hernández, T., Garcia, C., and Pascual, J. A. (1996). Stimulation of barley growth and nutrient absorption by humic substances originating from various organic materials. Bioresour. Technol. 57, 251–257. doi: 10.1016/S0960-8524(96)00064-68
Balmori, D. M., Domínguez, C. Y. A., Carreras, C. R., Rebatos, S. M., Farías, L. B. P., and Izquierdo, F. G. (2019). Foliar application of humic liquid extract from vermicompost improves garlic (Allium sativum L.) production and fruit quality. Int. J. Recycl. Organ. Waste Agric. 8, 103–112. doi: 10.1007/s40093-019-0279-271
Bettoni, M. M., Mogor, Á. F., Pauletti, V., Goicoechea, N., Aranjuelo, I., and Garmendia, I. (2016b). Nutritional quality and yield of onion as affected by different application methods and doses of humic substances. J. Food Compos. Anal. 51, 37–44. doi: 10.1016/j.jfca.2016.06.008
Bezuglova, O. S., Gorovtsov, A. V., Polienko, E. A., Zinchenko, V. E., Grinko, A. V., Lykhman, V. A., et al. (2019). Effect of humic preparation on winter wheat productivity and rhizosphere microbial community under herbicide-induced stress. J. Soils Sediments 19, 2665–2675. doi: 10.1007/s11368-018-02240-z
Bitton, G., Henis, Y., and Lahav, N. (1972). Effect of several clay minerals and humic acid on the survival of Klebsiella aerogenes exposed to ultraviolet irradiation. Appl. Microbiol. 23, 870–874. doi: 10.1128/aem.23.5.870-874.1972
Canellas, L. P., Canellas, N. O. A., Soares, T. S., and Olivares, F. L. (2018). Humic acids interfere with nutrient sensing in plants owing to the differential expression of TOR. J. Plant Growth Regul. 38, 216–224. doi: 10.1007/s00344-018-9835-9836
Canellas, L. P., and Olivares, F. L. (2017). Production of border cells and colonization of maize root tips by Herbaspirillum seropedicae are modulated by humic acid. Plant Soil 417, 403–413. doi: 10.1007/s11104-017-3267-3260
Canellas, L. P., Olivares, F. L., Aguiar, N. O., Jones, D. L., Nebbioso, A., and Mazzei, P. (2015b). Humic and fulvic acids as biostimulants in horticulture. Sci. Hortic. 196, 15–27. doi: 10.1016/j.scienta.2015.09.013
Canellas, L. P., Olivares, F. L., Canellas, N. O. A., Mazzei, P., and Piccolo, A. (2019). Humic acids increase the maize seedlings exudation yield. Chem. Biol. Technol. Agric. 6, 1–14. doi: 10.1186/s40538-018-0139-137
Canellas, L. P., Olivares, F. L., Okorokova-Façanha, A. L., and Façanha, A. R. (2002). Humic acids isolated from earthworm compost enhance root elongation, lateral root emergence, and plasma membrane H+-ATPase activity in maize roots. Plant Physiol. 130, 1951–1957. doi: 10.1104/pp.007088
Canellas, L. P., Spaccini, R., Piccolo, A., Dobbss, L. B., Okorokova-Façanha, A. L., and Santos, G. D. A. (2009). Relationships between chemical characteristics and root growth promotion of humic acids isolated from Brazilian oxisols. Soil Sci. 174, 611–620. doi: 10.1097/SS.0b013e3181bf1e03
Canellas, N. O. A., Olivares, F. L., and Canellas, L. P. (2019). Metabolite fingerprints of maize and sugarcane seedlings: searching for markers after inoculation with plant growth-promoting bacteria in humic acids. Chem. Biol. Technol. Agric. 6, 1–10. doi: 10.1186/s40538-019-0153-154
Çelik, H., Katkat, A. V., Aşik, B. B., and Turan, M. A. (2011). Effect of foliar-applied humic acid to dry weight and mineral nutrient uptake of maize under calcareous soil conditions. Commun. Soil Sci. Plant Anal. 42, 29–38. doi: 10.1080/00103624.2011.528490
Chen, Y., De Nobili, M., and Aviad, T. (2004). “Stimulatory effects of humic substances on plant growth,” in Soil Organic Matter in Sustainable Agriculture, eds F. Magdoff and R. Weil, (Boca Raton, FL: CRC Press), 131–165.
Cieschi, M. T., Polyakov, A. Y., Lebedev, V. A., Volkov, D. S., Pankratov, D. A., and Veligzhanin, A. A. (2019). Eco-friendly iron-humic nanofertilizers synthesis for the prevention of iron chlorosis in soybean (Glycine max) grown in calcareous soil. Front. Plant Sci. 10:413. doi: 10.3389/fpls.2019.00413
Da Silva, R. J., Ferreira Junior, J. M., Silva, F. A., Dos Santos, A. C. M., de Lima, S. O., et al. (2016). Humic substances, purified MAP and hydrogel in the development and survival of eucalyptus urograndis. Rev. Bras. Eng. Agric. Ambient. 20, 625–629. doi: 10.1590/1807-1929/agriambi.v20n7p625-629
Da Silva, S. F., Olivares, F. L., and Canellas, L. P. (2017). The biostimulant manufactured using diazotrophic endophytic bacteria and humates is effective to increase sugarcane yield. Chem. Biol. Technol. Agric. 4:24. doi: 10.1186/s40538-017-0106-108
D’Addabbo, T., Laquale, S., Perniola, M., and Candido, V. (2019). Biostimulants for plant growth promotion and sustainable management of phytoparasitic nematodes in vegetable crops. Agronomy 9:616. doi: 10.3390/agronomy9100616
Dawood, M. G., Abdel-Baky, Y. R., El-Awadi, M. E.-S., and Bakhoum, G. S. (2019). Enhancement quality and quantity of faba bean plants grown under sandy soil conditions by nicotinamide and/or humic acid application. Bull. Natl. Res. Cent. 43, 1–8. doi: 10.1186/s42269-019-0067-60
De Aquino, A. M., Canellas, L. P., da Silva, A. P. S., Canellas, N. O., Lima, L. S., and Olivares, F. L. (2019). Evaluation of molecular properties of humic acids from vermicompost by 13 C-CPMAS-NMR spectroscopy and thermochemolysis–GC–MS. J. Anal. Appl. Pyrolysis 141:104634. doi: 10.1016/j.jaap.2019.104634
De Azevedo, I. G., Olivares, F. L., Ramos, A. C., Bertolazi, A. A., and Canellas, L. P. (2019). Humic acids and Herbaspirillum seropedicae change the extracellular H+ flux and gene expression in maize roots seedlings. Chem. Biol. Technol. Agric. 6, 1–10. doi: 10.1186/s40538-019-0149-140
De Hita, D., Fuentes, M., García, A. C., Olaetxea, M., Baigorri, R., Zamarreño, A. M., et al. (2019). Humic substances: a valuable agronomic tool for improving crop adaptation to saline water irrigation. Water Sci. Technol. Water Supply 19, 1735–1740. doi: 10.2166/ws.2019.047
de Melo, D. M., Coelho, E. F., Borges, A. L., da Silva Pereira, B. L., and Campos, M. S. (2016). Agronomic performance and soil chemical attributes in a banana tree orchard fertigated with humic substances. Pesqui. Agropecuária Trop. 46, 421–428. doi: 10.1590/1983-40632016v4642222
Demir, K., Gunes, A., Inal, A., and Alpaslan, M. (1999). Effects of humic acids on the yield and mineral nutrition of cucumber (cucumis sativus l.) grown with different salinity levels. Acta Hortic. 492, 95–103. doi: 10.17660/actahortic.1999.492.11
Dobbss, L. B., Medici, L. O., Peres, L. E. P., Pino-Nunes, L. E., Rumjanek, V. M., and Façanha, A. R. (2007). Changes in root development of Arabidopsis promoted by organic matter from oxisols. Ann. Appl. Biol. 151, 199–211. doi: 10.1111/j.1744-7348.2007.00166.x
Drobek, M., Fra̧c, M., and Cybulska, J. (2019). Plant biostimulants: importance of the quality and yield of horticultural crops and the improvement of plant tolerance to abiotic stress-a review. Agronomy 9:335. doi: 10.3390/agronomy9060335
Erro, J., Urrutia, O., Baigorri, R., Fuentes, M., Zamarreño, A. M., and Garcia-Mina, J. M. (2016). Incorporation of humic-derived active molecules into compound NPK granulated fertilizers: main technical difficulties and potential solutions. Chem. Biol. Technol. Agric. 3, 1–15. doi: 10.1186/s40538-016-0071-77
Ertani, A., Francioso, O., Tugnoli, V., Righi, V., and Nardi, S. (2011). Effect of commercial lignosulfonate-humate on Zea mays L. metabolism. J. Agric. Food Chem. 59, 11940–11948. doi: 10.1021/jf202473e
Façanha, A. R., Façanha, A. L. O., Olivares, F. L., Guridi, F., Santos, G. D. A., and Velloso, A. C. X. (2002). Bioatividade de ácidos húmicos: efeitos sobre o desenvolvimento radicular e sobre a bomba de prótons da membrana plasmática. Pesqui. Agropecu. Bras. 37, 1301–1310. doi: 10.1590/s0100-204x2002000900014
Fallahi, H. R., Ghorbany, M., Aghhavani-Shajari, M., Samadzadeh, A., and Asadian, A. H. (2017). Qualitative response of roselle to planting methods, humic acid application, mycorrhizal inoculation and irrigation management. J. Crop. Improv. 31, 192–208. doi: 10.1080/15427528.2016.1269378
Fatma, K. M. S., Morsey, M. M., and Thanaa, S. M. (2015). Influence of spraying yeast extract and humic acid on fruit maturity stage and storability of “Canino” apricot fruits. Int. J. Chem. Tech Res. 8, 530–543.
Fernández-Escobar, R., Benlloch, M., Barranco, D., Dueñas, A., and Gutérrez Gañán, J. A. (1996). Response of olive trees to foliar application of humic substances extracted from leonardite. Sci. Hortic. 66, 191–200. doi: 10.1016/S0304-4238(96)00914-914
García, A. C., Quintero, J. J. P., Balmori, D. M., López, R. H., and Izquierdo, F. G. (2016a). Efeitos no cultivo do milho de um extrato líquido humificado residual, obtido a partir de vermicomposto. Rev. Ciencias Técnicas Agropecu. 25, 38–43.
García, A. C., Santos, L. A., de Souza, L. G. A., Tavares, O. C. H., Zonta, E., and Gomes, E. T. M. (2016b). Vermicompost humic acids modulate the accumulation and metabolism of ROS in rice plants. J. Plant Physiol. 192, 56–63. doi: 10.1016/j.jplph.2016.01.008
García, A. C., Santos, L. A., Izquierdo, F. G., Rumjanek, V. M., Castro, R. N., and dos Santos, F. S. (2014). Potentialities of vermicompost humic acids to alleviate water stress in rice plants (Oryza sativa L.). J. Geochem. Explor. 136, 48–54. doi: 10.1016/j.gexplo.2013.10.005
García, A. C., Santos, L. A., Izquierdo, F. G., Sperandio, M. V. L., Castro, R. N., and Berbara, R. L. L. (2012). Vermicompost humic acids as an ecological pathway to protect rice plant against oxidative stress. Ecol. Eng. 47, 203–208. doi: 10.1016/j.ecoleng.2012.06.011
García-Gaytán, V., Hernández-Mendoza, F., Coria-Téllez, A. V., García-Morales, S., Sánchez-Rodríguez, E., and Rojas-Abarca, L. (2018). Fertigation: nutrition, stimulation and bioprotection of the root in high performance. Plants 7, 1–13. doi: 10.3390/plants7040088
Gemin, L. G., Mógor, ÁF., De Oliveira Amatussi, J., and Mógor, G. (2019). Microalgae associated to humic acid as a novel biostimulant improving onion growth and yield. Sci. Hortic. 256:108560. doi: 10.1016/j.scienta.2019.108560
Giro, V. B., Jindo, K., Vittorazzi, C., De Oliveira, R. S. S., Conceição, G. P., and Canellas, L. P. (2016). Rock phosphate combined with phosphatesolubilizing microorganisms and humic substance for reduction of plant phosphorus demands from single superphosphate. Acta Hortic. 1146, 63–68. doi: 10.17660/ActaHortic.2016.1146.8
Hameed, A., Fatma, S., Wattoo, J. I., Yaseen, M., and Ahmad, S. (2018). Accumulative effects of humic acid and multinutrient foliar fertilizers on the vegetative and reproductive attributes of citrus (Citrus reticulata cv. kinnow mandarin). J. Plant Nutr. 41, 2495–2506. doi: 10.1080/01904167.2018.1510506
Hanafy Ahmed, A. H., Mohamed, H. F. Y., Orabi, I. O. A., and El-Hefny, A. M. (2018). Influence of gamma rays, humic acid and sodium nitroprusside on growth, chemical constituents and fruit quality of snap bean plants under different soil salinity levels. Biosci. Res. 15, 575–588.
Hernandez, O. L., Calderín, A., Huelva, R., Martínez-Balmori, D., Guridi, F., and Aguiar, N. O. (2014). Humic substances from vermicompost enhance urban lettuce production. Agron. Sustain. Dev. 35, 225–232. doi: 10.1007/s13593-014-0221-x
Hernandez, O. L., Huelva, R., Guridi, F., Olivares, F. L., and Canellas, L. P. (2013). Humatos isolados de vermicomposto como promotores de crescimento em cultivo orgânico de alface. Rev. Ciencias Técnicas Agropecu. 22, 70–75.
Ibrahim, E. A., and Ramadan, W. A. (2015). Effect of zinc foliar spray alone and combined with humic acid or/and chitosan on growth, nutrient elements content and yield of dry bean (Phaseolus vulgaris L.) plants sown at different dates. Sci. Hortic. 184, 101–105. doi: 10.1016/j.scienta.2014.11.010
Ibrahim, H. A. K. (2019). Effect of foliar application of compost water extract, humic acid, EDTA and micronutrients on the growth of fenugreek plants under sandy soil condition. Int. J. Environ. Sci. Technol. 16, 7799–7804. doi: 10.1007/s13762-019-02311-2319
Jindo, K., Soares, T. S., Peres, L. E. P., Azevedo, I. G., Aguiar, N. O., and Mazzei, P. (2016). Phosphorus speciation and high-affinity transporters are influenced by humic substances. J. Plant Nutr. Soil Sci. 179, 206–214. doi: 10.1002/jpln.201500228
Joshi, R., Singh, J., and Vig, A. P. (2014). Vermicompost as an effective organic fertilizer and biocontrol agent: effect on growth, yield and quality of plants. Rev. Environ. Sci. Biotechnol. 14, 137–159. doi: 10.1007/s11157-014-9347-9341
Juárez-Maldonado, A., Ortega-Ortíz, H., Morales-Díaz, A. B., González-Morales, S., Morelos-Moreno, Á., and Cabrera-De la Fuente, M. (2019). Nanoparticles and nanomaterials as plant biostimulants. Int. J. Mol. Sci. 20, 1–19. doi: 10.3390/ijms20010162
Justi, M., Morais, E. G., and Silva, C. A. (2019). Fulvic acid in foliar spray is more effective than humic acid via soil in improving coffee seedlings growth. Arch. Agron. Soil Sci. 65, 1969–1983. doi: 10.1080/03650340.2019.1584396
Kaiser, D., Bacher, S., Mène-Saffrané, L., and Grabenweger, G. (2019). Efficiency of natural substances to protect Beauveria bassiana conidia from UV radiation. Pest Manag. Sci. 75, 556–563. doi: 10.1002/ps.5209
Karakurt, Y., Unlu, H., Unlu, H., and Padem, H. (2009). The influence of foliar and soil fertilization of humic acid on yield and quality of pepper. Acta Agric. Scand. Sect. B Soil Plant Sci. 59, 233–237. doi: 10.1080/09064710802022952
Karimian, Z., Samiei, L., and Nabati, J. (2019). Alleviating the salt stress effects in Salvia splendens by humic acid application. Acta Sci. Pol. Hortorum Cultus 18, 73–82. doi: 10.24326/asphc.2019.5.7
Kaya, M., Atak, M., Khawar, K. M., Çiftçi, Cemalettin, Y., and Özcan, S. (2005). Effect of pre-sowing seed treatment with zinc and foliar spray of humic acids on yield of common bean (Phaseolus vulgaris L.). Int. J. Agric. Biol. 7, 875–878.
Kesba, H. H., and El-Beltagi, H. S. (2012). Biochemical changes in grape rootstocks resulted from humic acid treatments in relation to nematode infection. Asian Pac. J. Trop. Biomed. 2, 287–293. doi: 10.1016/S2221-1691(12)60024-0
Khan, R. U., Khan, M. Z., Khan, A., Saba, S., Hussain, F., and Jan, I. U. (2018). Effect of humic acid on growth and crop nutrient status of wheat on two different soils. J. Plant Nutr. 41, 453–460. doi: 10.1080/01904167.2017.1385807
Lewis, D. R., Ramirez, M. V., Miller, N. D., Vallabhaneni, P., Keith Ray, W., and Helm, R. F. (2011). Auxin and ethylene induce flavonol accumulation through distinct transcriptional networks. Plant Physiol. 156, 144–164. doi: 10.1104/pp.111.172502
Liu, Z., Gao, F., Yang, J., Zhen, X., Li, Y., and Zhao, J. (2019). Photosynthetic characteristics and uptake and translocation of nitrogen in peanut in a wheat–peanut rotation system under different fertilizer management regimes. Front. Plant Sci. 10:86. doi: 10.3389/fpls.2019.00086
Lotfi, R., Kalaji, H. M., Valizadeh, G. R., Khalilvand Behrozyar, E., Hemati, A., and Gharavi-Kochebagh, P. (2018). Effects of humic acid on photosynthetic efficiency of rapeseed plants growing under different watering conditions. Photosynthetica 56, 962–970. doi: 10.1007/s11099-017-0745-749
Maggioni, A., Varanini, V., Nardi, S., and Pinton, R. (1987). Action of soil humic matter on plant roots: stimulation of ion uptake and effects on (Mg2++K+) ATPase activity. Sci. Total Environ. 64, 334–336. doi: 10.1016/0048-9697(87)90257-90259
Maibodi, N. D. H., Kafi, M., Nikbakht, A., and Rejali, F. (2015). Effect of foliar applications of humic acid on growth, visual quality, nutrients content and root parameters of perennial ryegrass (Lolium Perenne L.). J. Plant Nutr. 38, 224–236. doi: 10.1080/01904167.2014.939759
Marques Júnior, R. B., Canellas, L. P., Da Silva, L. G., and Olivares, F. L. (2008). Promoção de enraizamento de microtoletes de cana-de-açúcar pelo uso conjunto de substâncias húmicas e bactérias diazotróficas endofíticas. Rev. Bras. Cienc. do Solo 32, 1121–1128. doi: 10.1590/S0100-06832008000300020
Martinez-Balmori, D., Spaccini, R., Aguiar, N. O., Novotny, E. H., Olivares, F. L., and Canellas, L. P. (2014). Molecular characteristics of humic acids isolated from vermicomposts and their relationship to bioactivity. J. Agric. Food Chem. 62, 11412–11419. doi: 10.1021/jf504629c
Masciandaro, G., Ceccanti, B., Ronchi, V., Benedicto, S., and Howard, L. (2002). Humic substances to reduce salt effect on plant germination and growth. Commun. Soil Sci. Plant Anal. 33, 365–378. doi: 10.1081/CSS-120002751
Masciandaro, G., Peruzzi, E., Doni, S., and Macci, C. (2014). Fertigation with wastewater and vermicompost: soil biochemical and agronomic implications. Pedosphere 24, 625–634. doi: 10.1016/S1002-0160(14)60048-60045
McLean, K. L., Hunt, J. S., Stewart, A., Wite, D., Porter, I. J., and Villalta, O. (2012). Compatibility of a Trichoderma atroviride biocontrol agent with management practices of Allium crops. Crop Prot. 33, 94–100. doi: 10.1016/j.cropro.2011.11.018
Melo, A., da, P., Olivares, F. L., Médici, L. O., Torres-Neto, A., Dobbss, L. B., et al. (2017). Mixed rhizobia and Herbaspirillum seropedicae inoculations with humic acid-like substances improve water-stress recovery in common beans. Chem. Biol. Technol. Agric. 4, 1–9. doi: 10.1186/s40538-017-0090-z
Merwad, A. R. M. A. (2017). Effect of humic and fulvic substances and Moringa leaf extract on Sudan grass plants grown under saline conditions. Can. J. Soil Sci. 97, 703–716. doi: 10.1139/cjss-2017-2050
Mohamadi, P., Razmjou, J., Naseri, B., and Hassanpour, M. (2017). Humic fertilizer and vermicompost applied to the soil can positively affect population growth parameters of Trichogramma brassicae (Hymenoptera: Trichogrammatidae) on Eggs of Tuta absoluta (Lepidoptera: Gelechiidae). Neotrop. Entomol. 46, 678–684. doi: 10.1007/s13744-017-0536-539
Monda, H., Cozzolino, V., Vinci, G., Drosos, M., Savy, D., and Piccolo, A. (2018). Molecular composition of the Humeome extracted from different green composts and their biostimulation on early growth of maize. Plant Soil 429, 407–424. doi: 10.1007/s11104-018-3642-3645
Motta, F. L., and Santana, M. H. A. (2013). Production of humic acids from oil palm empty fruit bunch by submerged fermentation with Trichoderma viride: cellulosic substrates and nitrogen sources. Biotechnol. Prog. 29, 631–637. doi: 10.1002/btpr.1715
Muscolo, A., Sidari, M., and Nardi, S. (2013). Humic substance: relationship between structure and activity. Deeper information suggests univocal findings. J. Geochem. Explor. 129, 57–63. doi: 10.1016/j.gexplo.2012.10.012
Nardi, S., Carletti, P., Pizzeghello, D., and Muscolo, A. (2009). Biological activities of humic substances. Biophys. Process. Involv. Nat. Nonliving Org. Matter Environ. Syst. 305–339. doi: 10.1002/9780470494950.ch8
Nardi, S., Concheri, G., Dell’Agnola, G., and Scrimin, P. (1991). Nitrate uptake and ATPase activity in oat seedlings in the presence of two humic fractions. Soil Biol. Biochem. 23, 833–836. doi: 10.1016/0038-0717(91)90094-Z
Nardi, S., Muscolo, A., Vaccaro, S., Baiano, S., Spaccini, R., and Piccolo, A. (2007). Relationship between molecular characteristics of soil humic fractions and glycolytic pathway and krebs cycle in maize seedlings. Soil Biol. Biochem. 39, 3138–3146. doi: 10.1016/j.soilbio.2007.07.006
Nardi, S., Pizzeghello, D., Gessa, C., Ferrarese, L., Trainotti, L., and Casadoro, G. (2000). A low molecular weight humic fraction on nitrate uptake and protein synthesis in maize seedlings. Soil Biol. Biochem. 32, 415–419. doi: 10.1016/S0038-0717(99)00168-166
Nikbakht, A., Kafi, M., Babalar, M., Xia, Y. P., Luo, A., and Etemadi, N. A. (2008). Effect of humic acid on plant growth, nutrient uptake, and postharvest life of gerbera. J. Plant Nutr. 31, 2155–2167. doi: 10.1080/01904160802462819
Nikbakht, A., Pessarakli, M., Daneshvar-Hakimi-Maibodi, N., and Kafi, M. (2014). Perennial ryegrass growth responses to mycorrhizal infection and humic acid treatments. Agron. J. 106, 585–595. doi: 10.2134/agronj2013.0275
Noroozisharaf, A., and Kaviani, M. (2018). Effect of soil application of humic acid on nutrients uptake, essential oil and chemical compositions of garden thyme (Thymus vulgaris L.) under greenhouse conditions. Physiol. Mol. Biol. Plants 24, 423–431. doi: 10.1007/s12298-018-0510-y
Nunes, R. O., Domiciano, G. A., Alves, W. S., Melo, A. C. A., Nogueira, F. C. S., and Canellas, L. P. (2019). Evaluation of the effects of humic acids on maize root architecture by label-free proteomics analysis. Sci. Rep. 9, 1–11. doi: 10.1038/s41598-019-48509-48502
Olaetxea, M., De Hita, D., Garcia, C. A., Fuentes, M., Baigorri, R., and Mora, V. (2018). Hypothetical framework integrating the main mechanisms involved in the promoting action of rhizospheric humic substances on plant root- and shoot- growth. Appl. Soil Ecol. 123, 521–537. doi: 10.1016/j.apsoil.2017.06.007
Olivares, F. L., Aguiar, N. O., Rosa, R. C. C., and Canellas, L. P. (2015). Substrate biofortification in combination with foliar sprays of plant growth promoting bacteria and humic substances boosts production of organic tomatoes. Sci. Hortic. 183, 100–108. doi: 10.1016/j.scienta.2014.11.012
Olivares, F. L., Busato, J. G., de Paula, A. M., da Silva Lima, L., Aguiar, N. O., and Canellas, L. P. (2017). Plant growth promoting bacteria and humic substances: crop promotion and mechanisms of action. Chem. Biol. Technol. Agric. 4:30.
Olk, D. C., Dinnes, D. L., Rene Scoresby, J., Callaway, C. R., and Darlington, J. W. (2018). Humic products in agriculture: potential benefits and research challenges—a review. J. Soils Sediments 18, 2881–2891. doi: 10.1007/s11368-018-1916-1914
Ozfidan-Konakci, C., Yildiztugay, E., Bahtiyar, M., and Kucukoduk, M. (2018). The humic acid-induced changes in the water status, chlorophyll fluorescence and antioxidant defense systems of wheat leaves with cadmium stress. Ecotoxicol. Environ. Saf. 155, 66–75. doi: 10.1016/j.ecoenv.2018.02.071
Parandian, F., and Samavat, S. (2012). Effects of fulvic and humic acid on anthocyanin, soluble Sugar, Amylase Enzyme and some micronurient elements in Lilium. Int. Res. J. Appl. Basic Sci. 3, 924–929.
Pinheiro, P. L., Passos, R. R., Peçanha, A. L., Canellas, L. P., Olivares, F. L., and de Sá Mendonça, E. S. (2018). Promoting the growth of Brachiaria decumbens by humic acids (HAs). Aust. J. Crop Sci. 12, 1114–1121. doi: 10.21475/ajcs.18.12.07.PNE1038
Pinos, N. Q., Berbara, R. L. L., Tavares, O. C. H., and García, A. C. (2019). Different structures in humic substances lead to impaired germination but increased protection against saline stress in corn. Commun. Soil Sci. Plant Anal. 50, 2209–2225. doi: 10.1080/00103624.2019.1659294
Pinto, J. M., Gava, C. A. T., Lima, M. A. C., Silva, A. F., and Resende, G. M. de (2008). Cultivo orgânico de meloeiro com aplicação de biofertilizantes e doses de substância húmica via fertirrigação. Rev. Ceres 55, 280–286.
Pinton, R., Varanini, Z., Vizzotto, G., and Maggioni, A. (1992). Soil humic substances affect transport properties of tonoplast vesicles isolated from oat roots. Plant Soil 142, 203–210. doi: 10.1007/BF00010966
Prado, M. R. V., Weber, O. L., dos, S., Moraes, M. F. de, Santos, C. L. R. dos, Tunes, M. S., et al. (2016). Humic Substances on soybeans grown under water stress. Commun. Soil Sci. Plant Anal. 47, 2405–2413. doi: 10.1080/00103624.2016.1243715
Pylak, M., Oszust, K., and Fra̧c, M. (2019). Review report on the role of bioproducts, biopreparations, biostimulants and microbial inoculants in organic production of fruit. Rev. Environ. Sci. Biotechnol. 18, 597–616. doi: 10.1007/s11157-019-09500-9505
Qin, K., Dong, X., Jifon, J., and Leskovar, D. I. (2019). Rhizosphere microbial biomass is affected by soil type, organic and water inputs in a bell pepper system. Appl. Soil Ecol. 138, 80–87. doi: 10.1016/j.apsoil.2019.02.024
Quaggiotti, S., Ruperti, B., Pizzeghello, D., Francioso, O., Tugnoli, V., and Nardi, S. (2004). Effect of low molecular size humic substances on nitrate uptake and expression of genes involved in nitrate transport in maize (Zea mays L.). J. Exp. Bot. 55, 803–813. doi: 10.1093/jxb/erh085
Rodda, C., Rita, M., Canellas, P., Façanha, R., Guerra, M., and Guilherme, J. (2006). Estímulo no crescimento e na hidrólise de ATP em raízes de alface tratadas com humatos de vermicomposto. I - Efeito da concentração. Rev. Bras. Ciência do Solo 30, 657–664.
Roomi, S., Masi, A., Conselvan, G. B., Trevisan, S., Quaggiotti, S., and Pivato, M. (2018). Protein profiling of arabidopsis roots treated with humic substances: insights into the metabolic and interactome networks. Front. Plant Sci. 871:1812. doi: 10.3389/fpls.2018.01812
Rosa, S. D., Silva, C. A., and Maluf, H. J. G. M. (2018). Wheat nutrition and growth as affected by humic acid-phosphate interaction. J. Plant Nutr. Soil Sci. 181, 870–877. doi: 10.1002/jpln.201700532
Rosa, S. D., Silva, C. A., and Maluf, H. J. G. M. (2019). Phosphorus availability and soybean growth in contrasting Oxisols in response to humic acid concentrations combined with phosphate sources. Arch. Agron. Soil Sci. 66, 220–235. doi: 10.1080/03650340.2019.1608527
Rose, M. T., Patti, A. F., Little, K. R., Brown, A. L., Jackson, W. R., and Cavagnaro, T. R. (2014). A Meta-Analysis and Review of Plant-Growth Response to Humic Substances: Practical Implications for Agriculture, 1st Edn. Amsterdam: Elsevier Inc, doi: 10.1016/B978-0-12-800138-7.00002-4
Russell, L., Stokes, A. R., Macdonald, H., Muscolo, A., and Nardi, S. (2006). Stomatal responses to humic substances and auxin are sensitive to inhibitors of phospholipase A2. Plant Soil 283, 175–185. doi: 10.1007/s11104-006-0011-16
Saa, S., Del Rio, A. O., Castro, S., and Brown, P. H. (2015). Foliar application of microbial and plant based biostimulants increases growth and potassium uptake in almond (Prunus dulcis [Mill.] D. A. Webb). Front. Plant Sci. 6:87. doi: 10.3389/fpls.2015.00087
Savy, D., Canellas, L., Vinci, G., Cozzolino, V., and Piccolo, A. (2017). Humic-Like water-soluble lignins from giant reed (Arundo donax L.) display hormone-like activity on plant growth. J. Plant Growth Regul. 36, 995–1001. doi: 10.1007/s00344-017-9696-9694
Schiavon, M., Pizzeghello, D., Muscolo, A., Vaccaro, S., Francioso, O., and Nardi, S. (2010). High molecular size humic substances enhance phenylpropanoid metabolism in maize (Zea mays L.). J. Chem. Ecol. 36, 662–669. doi: 10.1007/s10886-010-9790-9796
Schoebitz, M., López, M. D., Serri, H., Aravena, V., Zagal, E., and Roldán, A. (2019). Characterization of bioactive compounds in blueberry and their impact on soil properties in response to plant biostimulants. Commun. Soil Sci. Plant Anal. 50, 2482–2494. doi: 10.1080/00103624.2019.1667374
Seenivasan, N., and Senthilnathan, S. (2018). Effect of humic acid on Meloidogyne incognita (Kofoid & White) Chitwood infecting banana (Musa spp.). Int. J. Pest Manag. 64, 110–118. doi: 10.1080/09670874.2017.1344743
Selim, E. M., and Mosa, A. A. (2012). Fertigation of humic substances improves yield and quality of broccoli and nutrient retention in a sandy soil. J. Plant Nutr. Soil Sci. 175, 273–281. doi: 10.1002/jpln.201100062
Selim, E. M., Mosa, A. A., and El-Ghamry, A. M. (2009). Evaluation of humic substances fertigation through surface and subsurface drip irrigation systems on potato grown under Egyptian sandy soil conditions. Agric. Water Manag. 96, 1218–1222. doi: 10.1016/j.agwat.2009.03.018
Selladurai, R., and Purakayastha, T. J. (2016). Effect of humic acid multinutrient fertilizers on yield and nutrient use efficiency of potato. J. Plant Nutr. 39, 949–956. doi: 10.1080/01904167.2015.1109106
Smilkova, M., Smilek, J., Kalina, M., Klucakova, M., Pekar, M., and Sedlacek, P. (2019). A simple technique for assessing the cuticular diffusion of humic acid biostimulants. Plant Methods 15, 1–11. doi: 10.1186/s13007-019-0469-x
Smoleñ, S., Ledwożyw-Smoleñ, I., and Sady, W. (2017). Iodine biofortification of spinach by soil fertigation with additional application of humic and fulvic acids. New Zeal. J. Crop Hortic. Sci. 45, 233–250. doi: 10.1080/01140671.2017.1314307
Soppelsa, S., Kelderer, M., Casera, C., Bassi, M., Robatscher, P., and Matteazzi, A. (2019). Foliar applications of biostimulants promote growth, yield and fruit quality of strawberry plants grown under nutrient limitation. Agronomy 9, 1–22. doi: 10.3390/agronomy9090483
Souri, M. K., and Aslani, M. (2018). Beneficial effects of foliar application of organic chelate fertilizers on French bean production under field conditions in a calcareous soil. Adv. Hortic. Sci. 32, 265–272. doi: 10.13128/ahs-21988
Souri, M. K., and Sooraki, F. Y. (2019). Benefits of organic fertilizers spray on growth quality of chili pepper seedlings under cool temperature. J. Plant Nutr. 42, 650–656. doi: 10.1080/01904167.2019.1568461
Suman, S., Spehia, R. S., and Sharma, V. (2016). Productivity of capsicum as influenced by fertigation with chemical fertilizers and humic acid. J. Plant Nutr. 39, 410–416. doi: 10.1080/01904167.2015.1069338
Tanou, G., Ziogas, V., and Molassiotis, A. (2017). Foliar nutrition, biostimulants and prime-like dynamics in fruit tree physiology: new insights on an old topic. Front. Plant Sci. 8:75. doi: 10.3389/fpls.2017.00075
Tapia, Y., Casanova, M., Castillo, B., Acuña, E., Covarrubias, J., and Antilén, M. (2019). Availability of copper in mine tailings with humic substance addition and uptake by Atriplex halimus. Environ. Monit. Assess. 191:651. doi: 10.1007/s10661-019-7832-7832
Tarantino, A., Lops, F., Disciglio, G., and Lopriore, G. (2018). Effects of plant biostimulants on fruit set, growth, yield and fruit quality attributes of ‘Orange rubis§’ apricot® (Prunus armeniaca L.) cultivar in two consecutive years. Sci. Hortic. 239, 26–34. doi: 10.1016/j.scienta.2018.04.055
Tejada, M., and Gonzalez, J. L. (2003). Influence of foliar fertilization with amino acids and humic acids on productivity and quality of asparagus. Biol. Agric. Hortic. 21, 277–291. doi: 10.1080/01448765.2003.9755270
Tejada, M., Rodríguez-Morgado, B., Gómez, I., Franco-Andreu, L., Benítez, C., and Parrado, J. (2016). Use of biofertilizers obtained from sewage sludges on maize yield. Eur. J. Agron. 78, 13–19. doi: 10.1016/j.eja.2016.04.014
Toropkina, M. A., Ryumin, A. G., Kechaikina, I. O., and Chukov, S. N. (2017). Effect of humic acids on the metabolism of Chlorella vulgaris in a model experiment. Eurasian Soil Sci. 50, 1294–1300. doi: 10.1134/S1064229317110126
Trevisan, S., Manoli, A., Begheldo, M., Nonis, A., Enna, M., Vaccaro, S., et al. (2011). Transcriptome analysis reveals coordinated spatiotemporal regulation of hemoglobin and nitrate reductase in response to nitrate in maize roots. New Phytol. 192, 338–352. doi: 10.1111/j.1469-8137.2011.03822.x
Van Oosten, M. J., Pepe, O., De Pascale, S., Silletti, S., and Maggio, A. (2017). The role of biostimulants and bioeffectors as alleviators of abiotic stress in crop plants. Chem. Biol. Technol. Agric. 4, 1–13. doi: 10.1186/s40538-017-0089-85
Waqas, M., Ahmad, B., Arif, M., Munsif, F., Latif Khan, A., and Amin, M. (2014). Evaluation of humic acid application methods for yield and yield components of Mungbean. Am. J. Plant Sci. 5, 2269–2276. doi: 10.4236/ajps.2014.515241
Xu, D., Deng, Y., Xi, P., Yu, G., Wang, Q., and Zeng, Q. (2019). Fulvic acid-induced disease resistance to Botrytis cinerea in table grapes may be mediated by regulating phenylpropanoid metabolism. Food Chem. 286, 226–233. doi: 10.1016/j.foodchem.2019.02.015
Yang, W., Guo, S., Li, P., Song, R., and Yu, J. (2019). Foliar antitranspirant and soil superabsorbent hydrogel affect photosynthetic gas exchange and water use efficiency of maize grown under low rainfall conditions. J. Sci. Food Agric. 99, 350–359. doi: 10.1002/jsfa.9195
Zaller, J. G. (2006). Foliar spraying of vermicornpost extracts: effects on fruit quality and indications of late-blight suppression of field-grown tomatoes. Biol. Agric. Hortic. 24, 165–180. doi: 10.1080/01448765.2006.9755017
Zandonadi, D. B., Canellas, L. P., and Façanha, A. R. (2007). Indolacetic and humic acids induce lateral root development through a concerted plasmalemma and tonoplast H+ pumps activation. Planta 225, 1583–1595. doi: 10.1007/s00425-006-0454-452
Zandonadi, D. B., Matos, C. R. R., Castro, R. N., Spaccini, R., Olivares, F. L., and Canellas, L. P. (2019). Alkamides : a new class of plant growth regulators linked to humic acid bioactivity. Chem. Biol. Technol. Agric. 4, 1–12. doi: 10.1186/s40538-019-0161-164
Zandonadi, D. B., Santos, M. P., Busato, J. G., Peres, L. E. P., and Façanha, A. R. (2013). Plant physiology as affected by humified organic matter. Theor. Exp. Plant Physiol. 25, 13–25. doi: 10.1590/s2197-00252013000100003
Zanin, L., Tomasi, N., Cesco, S., Varanini, Z., and Pinton, R. (2019). Humic substances contribute to plant iron nutrition acting as chelators and biostimulants. Front. Plant Sci. 10:675. doi: 10.3389/fpls.2019.00675
Zanin, L., Tomasi, N., Zamboni, A., Sega, D., Varanini, Z., and Pinton, R. (2018). Water-extractable humic substances speed up transcriptional response of maize roots to nitrate. Environ. Exp. Bot. 147, 167–178. doi: 10.1016/j.envexpbot.2017.12.014
Zhang, H., Xie, S., Bao, Z., Tian, H., Carranza, E. J. M., and Xiang, W. (2019). Underlying dynamics and effects of humic acid on selenium and cadmium uptake in rice seedlings. J. Soils Sediments 20, 109–121. doi: 10.1007/s11368-019-02413-2414
Keywords: humic acid, fulvic acid, foliar application, fertigation, circular economy, sustainable agriculture
Citation: Jindo K, Olivares FL, Malcher DJP, Sánchez-Monedero MA, Kempenaar C and Canellas LP (2020) From Lab to Field: Role of Humic Substances Under Open-Field and Greenhouse Conditions as Biostimulant and Biocontrol Agent. Front. Plant Sci. 11:426. doi: 10.3389/fpls.2020.00426
Received: 28 January 2020; Accepted: 24 March 2020;
Published: 12 May 2020.
Edited by:Andrew Merchant, University of Sydney, Australia
Reviewed by:Jose M. Garcia-Mina, University of Navarra, Spain
Barbara De Lucia, University of Bari Aldo Moro, Italy
Copyright © 2020 Jindo, Olivares, Malcher, Sánchez-Monedero, Kempenaar and Canellas. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
*Correspondence: Miguel Angel Sánchez-Monedero, firstname.lastname@example.org