Next Article in Journal
The Hotspots and Trends in the Literature on Cleaner Production: A Visualized Analysis Based on Citespace
Previous Article in Journal
Research Topic Specialization of Universities in Information Science and Library Science and Its Impact on Inter-University Collaboration
Previous Article in Special Issue
Nitrogen Uptake, Use Efficiency, and Productivity of Nigella sativa L. in Response to Fertilization and Plant Density
 
 
Search for Articles:
Title / Keyword
Author / Affiliation / Email
Journal
Article Type
 
 
Advanced Search
 
Section
Special Issue
Volume
Issue
Number
Page
 
Journals
Sustainability
Volume 14
Issue 15
10.3390/su14159001
sustainability-logo
Submit to this Journal Review for this Journal Propose a Special Issue
► Article Menu

Article Menu

share Share announcement Help format_quote Cite question_answer Discuss in SciProfiles thumb_up
...
Endorse textsms
...
Comment
first_page
settings
Order Article Reprints
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:
Background:
Article

The Influence of Arbuscular Mycorrhizal Fungus Rhizophagus irregularis on the Growth and Quality of Processing Tomato (Lycopersicon esculentum Mill.) Seedlings

by
Ioannis Roussis
1,
Dimitrios Beslemes
2,
Chariklia Kosma
3,
Vassilios Triantafyllidis
3,
Anastasios Zotos
4,
Evangelia Tigka
5,
Antonios Mavroeidis
1,
Stella Karydogianni
1,
Varvara Kouneli
1,
Ilias Travlos
1 and
Ioanna Kakabouki
1,*
1
Laboratory of Agronomy, Department of Crop Science, Agricultural University of Athens, 11855 Athens, Greece
2
Research and Development Department, Alfa Seeds ICSA, 41500 Larissa, Greece
3
Department of Business Administration of Food and Agricultural Enterprises, University of Patras, 30100 Agrinio, Greece
4
Department of Biosystems and Agricultural Engineering, University of Patras, 30200 Mesolonghi, Greece
5
Institute of Industrial and Forage Crops, Hellenic Agricultural Organization Demeter, 41335 Larissa, Greece
*
Author to whom correspondence should be addressed.
Sustainability 2022, 14(15), 9001; https://doi.org/10.3390/su14159001
Submission received: 20 May 2022 / Revised: 20 July 2022 / Accepted: 21 July 2022 / Published: 22 July 2022
(This article belongs to the Special Issue Soil Fertility Improvement and Integrated Nutrient Management—a Pathway to Sustainable Agriculture)
Browse Figure
Versions Notes

Abstract

:
Tomato (Lycopersicon esculentum Mill.) is one of the most valuable horticultural crops, not only for its economic importance but also for its high nutritional value and sensory qualities. The arbuscular mycorrhiza (AM) fungus Rhizophagus irregularis can improve plant nutrient uptake and decrease seedling transplanting shock. Although R. irregularis is one of the most extensively studied AMF species, there is a paucity of data on the effects of this species on processing tomato seedlings produced in an aerated hydroponic float system. A greenhouse experiment with four treatments and three replications was established in a completely randomized design. The treatments contained the addition of 0, 40, 80, and 120 fungal spores per L of nutrient solution (control, AMF1, AMF2, and AMF3, respectively). Root colonization analysis proved that the maximum dose of applied AMF (AMF3) supported colonization to a large extent, succeeding 36.74%. In addition, the highest values of total dry weight (1.386 g), survival rate (94.79%), N content (3.376 mg per 100 g DW) and P content (0.497 mg per 100 g DW) were also observed under AMF3 treatment. In conclusion, the application of high doses of the AM fungus R. irregularis in nutrient solutions of float system leads to a substantial improvement in the quality and growth of processing tomato seedlings.

1. Introduction

Tomato (Lycopersicon esculentum Mill.) constitutes the second most widely produced and consumed vegetable crop, after potato, and the worldwide production has been estimated at 186 million tonnes per year from a total cultivation area of around 5.1 million hectares [1]. Due to its high levels of antioxidants, it is suggested that an adult human consumes 25 to 32 kg of tomatoes per year [2]. Tomatoes are ingested in the form of both fresh and processed products. A percentage higher than 80% of the tomatoes cultivated worldwide are processed into products such as sauce, juice, ketchup, canned tomato, stew, and soup [2,3]. Increased productivity and fruit quality are required for successful processing tomato production. In the Mediterranean countries, where tomato growing requirements are large in water and fertilization inputs, cropping practices should be enhanced to improve the sustainability of processing tomato production while retaining high levels of yield to meet the demands of an expanding population [4]. Under the present climate change scenarios, rising temperatures and variations in precipitation intensity and distribution would exacerbate heat and drought related stresses, reducing crop productivity [5,6].
Conventional plant breeding and genetic engineering were used to develop stress tolerant cultivars in research to enhance drought resilience and alleviate the negative impacts of climate change on crop productivity, with little attention paid to the complex ecological interactions, particularly at the soil level [7,8,9]. Among plant growth promoting microorganisms (PGPM), arbuscular mycorrhizal fungi (AMF) have been frequently recorded to enhance abiotic stress tolerance in plant species. AMF create a mutualistic symbiotic interaction with the roots of most terrestrial plants, including the tomato plant, by forming typical intracellular fungal structures in the root cortex called arbuscules, which are believed to be the location of nutrient transfers among the partners [6,10]. Furthermore, being obligate biotrophs, AMF consume carbon compounds from the host plant in exchange for water and low transportable nutrients, such as phosphorus, hence extending the root depletion zone via their extraradical hyphae [11,12]. The symbiosis of plants with AMF often results in enhanced levels of tolerance to abiotic stress, such as drought, salinity, nutrient deficiency, heavy metals and adverse soil pH, as described in literature [13,14,15,16]. In particular, under drought conditions, AMF inoculation in maize plants increased growth and photosynthetic activity by improving chlorophyll content, nutrient uptake and assimilation [17]. In response to a water deficient environment, higher plant heights, root length, and vigor, as well as mineral nutrient leaf concentrations (NO3−, PO43−, SO42−, and Na+), attributable to key tolerance mechanisms and upregulating antioxidant enzyme activities were found in durum wheat inoculated plants [18]. Enhanced fruit yield of AMF inoculated tomatoes was also found for the most efficient maintenance of leaf water potential and nutritional status with increased nitrogen (N) and phosphorus (P) content [6,13,19].
Currently, contemporary cropping practices have eventuated in a decrease in diversity and frequency of AM fungi in agricultural soils and potting soil substrates, a consequence attributed to tillage methods, mineral fertilizer use as well as nursery substrate sterilization, among other factors [12]. As a result, AM fungal spores have been applied externally, with AMF inoculum added to seedlings’ growing medium or into the planting hole at the time of transplanting. Therefore, two major agronomic benefits are anticipated: (a) greater seedling growth in the nursery and (b) increased production of mature plants succeeding field planting [9,20].
Hydroponic systems, such as the float system, are commonly used to cultivate seedlings of a large number of cultivated plant species, including vegetables (i.e., tomato), tobacco, and cannabis [21,22,23]. Cultivation in a typical float system is frequently conducted on Styrofoam sheets that float on top of troughs filled with nutrient solutions [24]. Nutrient solutions, which can be either organic or inorganic in nature, have a significant impact on plant growth [25]. In addition, it should be noted that plants grown on float systems typically have a substantially larger root system [26,27]. As the root length, diameter, and density are mainly related to the plant uptake rates for water and nutrients, the float system seedlings present high-quality attributes [28,29]. Furthermore, Dickson’s quality index (DQI) can be utilized to assess seedling quality by evaluating root biomass and other agronomic properties [30].
The inclusion of AMF in nutrient solutions of float systems could be advantageous for processing tomato seedlings. AMF include a variety of fungal species from the Glomaceae family [31]. Particular attention has been paid to the effects of Rhizophagus irregularis (syn. Glomus intraradices) on tomato plants grown in various cultivation systems [6,9,32,33]. With relevance to these research works, the existence of the previously mentioned fungi on plant roots compensated for the detrimental effects of abiotic stress and enhanced nutritional quality. Although there is research available on the application of the AM fungus R. irregularis on tomato plants, there is a paucity of evidence on the effects of R. irregularis on processing tomato seedlings produced in a float system. The current research work intends to examine, for the first time to our knowledge, the AM fungus R. irregularis effect on the growth and quality of processing tomato seedlings grown on a float system using Dickson’s Quality Index.

2. Materials and Methods

An experiment was conducted in a glasshouse at the Agricultural University of Athens (37°58′55.83″ N, 23°42′16.69″ E) from April to May 2018 to assess the influence of the AM fungus Rhizophagus irregularis on the growth and quality of processing tomato seedlings. The average lowest and highest recorded temperatures during the experiment was 14.3 °C and 36.1 °C, respectively (average 15.2 °C). The relative humidity (RH) reached from 45% to 81% (average 70%). For the experiment, arranged according to a completely randomized design (CRD), four treatments with three replications per treatment were employed. The treatments included the application of 0, 40, 80, and 120 fungal spores per L of nutrient solution (control, AMF1, AMF2, and AMF3, respectively; Table 1).
At first, polystyrene floating trays with 150 cells per tray (individual cell volume 12 cm3) were filled with a mixture of organic peat and vermiculite 1:1 v/v. On each individual cell, one seed of processing tomato (Lycopersicon esculentum Mill. cv. Heinz 3402 F1) was hand-sown on 9 April 2018 by placing the seed on the surface of the substrate, without additional covering. The trays were then put into 50 L troughs filled with tap water, where two trays were put into each trough. In the current study, twelve troughs of equal size were utilized for the floating system: three for each treatment (4 treatments × 3 troughs). In all troughs, 1 L of organic water-soluble fertilizer Fish–Fert (2–4–0.5 and other trace elements) (Humofert S.A., Athens, Greece) was added and its chemical composition is presented in Table 2. With the exception of the control treatment, the nutrient solution of each trough received various doses of the commercial root inoculant product MycoPlant® Polvo Grow (Tratamientos BioEcológicos S.A., Murcia, Spain), which contained water–dispersible granules of R. irregularis. The number of fungal spores added to each trough is presented in Table 1. The choice of the root inoculant product doses to be tested was based on the dosage of 0.15 g per L of nutrient solution recommended by the manufacturer for tomato, adding quantities below and above the recommended. In addition, the nutrient solution in the troughs was aerated with an air pump (EcoPlus 728459; Intertek, Shanghai, China) pumping 3566 GPH and with a diaphragm and filter in order to prevent dust from entering the solution. Aeration was maintained 24 h a day during the duration of the experiment and allowed a dissolved oxygen (DO) concentration of 6.4 mg L−1 (Microprocessor Dissolved Oxygen meter HI 9146; HANNA Instruments, Woonsocket, RI, USA). The seedlings emerged 10 days after sowing with a germination percentage of 91% and were transplanted in the field at 30 days after their emergence (DAE).
The traits that were taken into account in order to assess the processing tomato seedlings were the plant biometric parameters, nitrogen (N) and phosphorus (P) content, as well as the survival rate. Besides the survival rate, all other measurements necessitated destructive sampling. As a result, 20 seedlings from each treatment were collected at 25 DAE, and the following plant biometric parameters were evaluated: plant height, dry weight of the plant aboveground parts (shoot) and roots, stem diameter and total root length. Shoot length was measured from the substrate surface to the apical bud of the plant. For the determination of dry weight, the samples were oven-dried for 72 h at 64 °C. The stem diameter and total root length were measured by placing the collected samples on a high-resolution scanner (HP Scanjet 200 Flatbed Photo Scanner; Hewlett-Packard Inc., Palo Alto, CA, USA) using Delta–Τ software (Delta–Τ Scan ver. 2.04; Delta–Τ Devices Ltd., Burwell, Cambridge, UK) (Figure S1). The current parameters were then applied to define Dickson’s quality index (DQI) described by Dickson et al. [34], as follows:
DQI = Seedling   total   dry   weight   g Shoot   length   cm Shoot   diameter   cm + Shoot   dry   weight   g Root   dry   weight   g
The total N content was determined by grinding the dried samples to a fine powder and applying them to the Kjeldahl procedure using a Kjeltec 8400 autoanalyzer (Foss Tecator AB, Höganas, Sweden). Moreover, for the measurement of the P content, ten plants per treatment were also harvested at 25 DAE, dissolved in an HNO3H2O2 solution, and heated under pressure in a CEM MDS-2000 microwave digestor oven (CEM Microwave Technology Ltd., Buckingham, UK). The extract was consequently analyzed using an iCAP 6500 DUO inductively coupled plasma emission spectrometer (Thermo Fisher Scientific, Waltham, MA, USA). The survival rate was evaluated by sight at 25 DAE. In addition, the percentage of root length colonized by the arbuscular mycorrhizal fungi (AMF) was also determined microscopically at 5, 9, 13, 17, 21 and 25 DAE with the gridline-intersection method at a 30–40× magnification [35] after cleaning washed roots in 10% (w/v) KOH for 10 min at 90 °C and staining with 0.05% (w/v) trypan blue dissolved in lactophenol [36].
The experimental data were statistically analyzed using the SigmaPlot 12 statistical program (Systat Software Inc., San Jose, CA, USA) according to the completely randomized design (CRD). One-way ANOVA was used to examine the significance of the data, and differences among means were separated using Tukey’s honestly significant difference (Tukey’s HSD) test. All comparisons were made at the level of probability (p ≤ 0.05).

3. Results

3.1. Mycorrhizal Functioning

The analysis of root colonization revealed that the untreated seedlings presented the lowest mycorrhizal infection. In particular, the arbuscular mycorrhizal fungi (AMF) colonization on untreated processing tomato seedlings was kept below 8% for the first twenty-five days after the emergence of seedlings (Figure 1). Significant variations were observed among regimes, with the inclusion of the AMF appearing to enhance mycorrhizal colonization in roots. Between the three distinct AMF treatments, the highest dose examined (AMF3) supported colonization to a larger extent, achieving 36.74%. On the other hand, the medium (AMF2) and minimum (AMF1) doses presented statistically lower values in comparison to AMF3, with the values being 28.77% and 24.20%, respectively.

3.2. Seedlings Growth and Development

The presence of AM fungus R. irregularis influenced both the growth of aboveground parts and roots of processing tomato seedlings. After the AMF application, significant variation in total root length was found among treated and untreated plants. Especially, the highest total root length was found in the case of maximum AMF dose (AMF3) with the length increased by 54.72% compared to the control seedlings. In the same manner, the root dry weight of AMF3 treated plants was 54.19% higher in contrast to the non-treated plants (Table 3).
In terms of the growth of processing tomato aboveground parts, the addition of AMF in nutrient solution had no influence on the shoot length and stem diameter (Table 3). On the contrary, the enhancement of AMF resulted in a considerable increase in shoot dry weight. As a result, tomato plants exposed to the maximum AMF dose (AMF3) had the highest dry weight (1.113 g), whereas untreated (control) plants had the lowest (0.675 g).
The root to shoot ratio was not significantly affected by AMF treatments during the experiment. The higher R. irregularis rates favored the seedling total dry weight with the highest value (1.386 g) obtained in the maximum AMF dose (AMF3) followed by AMF2 (1.206 g) and AMF1 (1.097 g) treatments, while the lowest value (0.855 g) was observed in the untreated plants (Table 3). Consequently, the findings of the current investigation support the hypothesis that AMF colonization stimulates plant development.
The experiment results indicated that the medium and maximum AMF doses (AMF2 and AMF3, respectively) had a favorable effect on the plant’s nitrogen (N) content, with values being 24.39% and 16.61% greater than the control treatment (Table 4). Furthermore, the phosphorus (P) content of the tomato seedlings was also increased with the AMF augmentation, and the greatest value (0.497 mg 100 g−1 DW) recorded in AMF3 treatment followed by AMF2 and AMF1 (0.463 and 0.434 mg 100 g−1 DW, respectively) treatments.
Similarly, Dickson’s quality index (DQI) was significantly affected by the increased rates of R. irregularis, and the highest values were observed in maximum (0.198) and medium dose (0.177) of AMF (Table 4). Moreover, statistically significant differences were observed for the survival rate, where the highest values observed in AMF3 (94.78%) and AMF 2 (93.74%) treatments.

4. Discussion

AMF colonization has been shown to play an essential role in stimulating plant development and seedling quality [37,38]. AMFs’ ability to promote plant growth can be shown in a variety of parameters and plant tissues, such as biomass accumulation [39,40]. In the current study, the impacts of AMF colonization on plants were clearly demonstrated after the inoculation with R. irregularis on processing tomato seedlings.
Rhizophagus irregularis promoted processing tomato root growth by enhancing total root length and dry weight. The inoculated seedlings with the highest AMF dose (AMF3) presented almost 50% higher total root length as compared to the non–inoculated seedlings, which might probably enhance nutrient uptake and better growth in the field. Previous studies confirm the present results, describing a beneficial effect of R. irregularis on the root development and biomass of tomato plants [6,9,13,19,32]. In general, it is well accepted that inoculation during the early stages of plant development can promote AM symbiosis, resulting in enhanced plant growth in the nursery and improved field performance after planting [9,37,38,41].
Plant growth parameters, including stem length, stem diameter as well as biomass production, are the external indicators of internal plant metabolism. Throughout the study period, the abovementioned parameters of inoculated seedlings remained consistently higher than those of non–mycorrhizal seedlings (Table 3). These results are in accordance with Fracasso et al. [6] and Kakabouki et al. [23], who observed significantly increased shoot length, stem diameter, and shoot dry weight upon inoculation with R. irregularis in tomato and cannabis plants, respectively.
In addition, the application of AMF increased the root to shoot ratio in inoculated plants. This revealed that AMF-inoculated seedlings divided more biomass to the roots than to the shoots, implying that AMF inoculation may have increased the nutritional absorption area in AMF–colonized seedlings. According to Begum et al. [38], a higher root to shoot ratio indicated a high level of mycorrhizal efficacy. A betterment in seedling quality seen in terms of growth characteristics when compared to the control further endorsed the notion that the infected seedlings enhanced their vigor, robustness, and development, and hence transplanting performance. AMF was found to be beneficial to tomato seedlings inoculated with R. irregularis [9,13]. Moreover, mycorrhizal inoculation has been found to promote crop uniformity, reduce transplant mortality, and increase the production of many horticultural crops in soilless substrates lacking AM fungi [15,37].
These findings show a substantial positive relationship between AMF root colonization and plant biometric characteristics including the development of roots and whole-plant dry biomass of processing tomato seedlings (Table 5). Considering the rate of AMF root colonization, this feature may become increasingly apparent. In cases with greater amounts of R. irregularis, the colonization rate was actually higher, resulting in a more intensive symbiotic relationship among AMF and the host plant. The abovementioned mechanism promotes root system reinforcement and, as a result, enhances plant growth [42].
Remarkably, the mycorrhizal symbiosis reported in this study seems to have a significant influence on seedling nutrient uptake. Concerning the phosphorus (P), R. irregularis increased the availability of this mineral in the rhizosphere and improved its uptake by processing tomato seedlings, with the greatest results detected in seedlings inoculated with the highest AMF dose (AMF3) (Table 4). Although P is not readily available to plants due to its low solubility, processes such as extracellular phosphatase mineralization as well as mycorrhizal fungus solubilization make P available to seedlings [43,44]. As a result, P, as a required component for plant metabolism and growth, has the potential to play a key role in critical physiological functions. [23,45]. P sufficiency is even more important in plant species such as processing tomatoes, where P deficiency may have a deleterious impact on reproductive organs and inflorescence initiation [45].
As for the nitrogen (N) accumulation, increasing the AMF dose had also a favorable effect. The N content in processing tomato seedlings with AMF inoculation might be related the AMF extraradical mycelium’s ability to control N uptake into intra-mycelium and, ultimately, to the host plant [46]. Several studies have demonstrated that the AMF can transfer approximately 20–75 percent of the total N uptake to their hosts’ plants [47,48,49,50].
The inoculation with AM fungus R. irregularis has been demonstrated to induce a higher photosynthetic ability of seedlings of diverse plant species [37,38]. Enhanced photosynthesis might be one of the elements that accounts for the reported increased total dry mass production of processing tomato seedlings. The enhanced N uptake and content related to AMF colonization clearly results in increased levels of chlorophyll (the primary pigment used in photosynthesis), since chlorophyll molecules can effectively trap N [51]. In addition, induced P availability in plants related to AMF colonization may have an indirect effect on photosynthesis by changing the ratio of ATP to ADP or the activity of the enzyme ribulose 1,5-bisphosphate (RuBP) carboxylase [52]. The present explanation is consistent with the higher P content in the plant seedlings, which the current data additionally revealed. Furthermore, R. irregularis has the ability to increase PEPCase activity, an enzyme involved in malate production [53,54]. Malate constitutes the final product of the photosynthetic carbon reduction (PCR) cycle in C3 plants such as tomato, proving that R. irregularis has a fundamental effect on photosynthesis.
However, it is worth highlighting that greater nutrition and higher photosynthetic rates may not be the only causes for the seedlings’ overall enhanced the survival rate as well as the seedlings’ quality. In addition to their effects on plant nutrient uptake, AMF has been reported to increase the production of phytohormones [55]. Specifically, the application of two AMF species (Glomus mosseae and Glomus intraradices) on tomato plants substantially increased salicylic acid levels in mycorrhizal roots compared to nonmycorrhizal controls [56]. In addition to its role in stress-relieving pathways, salicylic acid has been shown to affect seed germination and seedling establishment [57].
In addition, literature has shown that R. irregularis helps minimize transplanting shock on seedlings. [37,38,58]. In a research study that investigated the influence of several AMF species (including Glomus sp.) on micropropagated grapevine plantlets, it was found that AMF colonization was an efficient technique to reduce the shock of transplantation [59]. Specifically, it was observed that mycorrhizal plants produced more proline, a nonprotein amino acid that forms in the majority of plant tissues experiencing stress conditions [60]. Various surveys on the importance of proline in osmotic adjustment and protein protection under stress conditions support this claim [38,61]. Irrespectively of proline quantities, transplanting shock endurance is greatly assigned to a well-developed root system that is capable of supporting the plant, facing environmental changes, and absorbing adequate nutrients and water [62].
Although the accumulation of biochemical compounds, such as salicylic acid and proline, was not assessed in the present study, AMF actually improved root growth and development. The possibility of AMF–induced phytohormones, proteins, and other biological substances influencing processing tomato seedling quality should not be disregarded. More research is required on the reciprocal influence of R. irregularis, its metabolites, and the processing tomato metabolic pathways that they may activate, resulting in robust seedlings.
Considering Dickson’s quality index (DQI), the strong relationship between this index and AMF recorded in the current research (Table 4) is consistent with the majority of the literature. Researchers have previously utilized DQI to investigate the influence of AMFs on seedling quality in a variety of plant species [30,63,64,65]. Moreover, DQI as an indicator of robustness and plant biomass [66], presented a significant and strong correlation with biometric characteristics of processing tomato seedlings (Table 5). However, the total N and P concentration in the seedlings appears to alter DQI (Table 5), showing that nutrition may affect the index values. Finally, despite the present interaction, the research findings show that DQI can be used to impartially assess the quality of processing tomato seedlings.

5. Conclusions

In the current study, the inoculation with AM fungus R. irregularis as a PGPM influenced the biometrical characteristics of the above and belowground processing tomato tissues. Specifically, the total root length, as well as the seedling total dry weight of processing tomato were significantly increased. Moreover, the mycorrhizal symbiosis positively affected nutrient uptake by the seedlings with the highest accumulation of nitrogen and phosphorus recorded in the AMF3 treatment. Furthermore, R. irregularis improved the stress resistance of seedlings, resulting in a significant increase in survival rate. In conclusion, the application of high doses of the AM fungus R. irregularis in nutrient solutions of float system leads to a substantial improvement in the quality and growth of processing tomato seedlings. In addition, more research into the mechanisms and biochemical pathways is needed to underline the beneficial interaction between R. irregularis and processing tomato seedlings grown in a float system.

Supplementary Materials

The following supporting information can be downloaded at: https://www.mdpi.com/article/10.3390/su14159001/s1, Figure S1: Images of the working window of the Delta–Τ Scan software.

Author Contributions

Conceptualization, I.R. and I.K.; methodology, I.R., D.B., C.K., V.T., A.Z., E.T., A.M., S.K., V.K., I.T. and I.K.; validation, I.R., I.K. and D.B.; formal analysis, I.R. and I.K.; investigation, I.R., D.B., C.K., V.T., A.Z., E.T., A.M., S.K., V.K., I.T. and I.K.; resources, I.R., I.K. and A.M.; writing—original draft preparation, I.R. and I.K.; writing—review and editing, I.R. and I.K.; supervision I.R., I.T. and I.K. All authors have read and agreed to the published version of the manuscript.

Funding

This work was supported by EU ERANET–MANUNET II program “SusTainable explOitation of toMATO proCessing industrY by-produCts (TOMATOCYCle)” funded under the RIS3 Priority Sector Support “Development of Transnational Research Projects for Small and Medium–Sized Enterprises” under the Operational Program “Western Greece 2014–2020. EU MANUNET”, project no. 34 ERANET/2017-UEFISCDI-MCI.

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

The data presented in this study are available on request from the corresponding author.

Conflicts of Interest

The authors declare no conflict of interest. The funders had no role in the design of the study; in the collection, analyses, or interpretation of data; in the writing of the manuscript; or in the decision to publish the results.

References

  1. FAOSTAT. Food and Agriculture Organization of the United Nations. 2020. Available online: https://www.fao.org/faostat/en/#data/QCL (accessed on 1 April 2022).
  2. Viskelis, P.; Radzevicius, A.; Urbonaviciene, D.; Viskelis, J.; Karkleliene, R.; Bobinas, C. Biochemical parameters in tomato fruits from different cultivars as functional foods for agricultural, industrial, and pharmaceutical uses. In Plants for the Future; El Shemy, H., Ed.; IntechOpen: London, UK, 2015. [Google Scholar] [CrossRef] [Green Version]
  3. Bilalis, D.; Krokida, M.; Roussis, I.; Papastylianou, P.; Travlos, I.; Cheimona, N.; Dede, A. Effects of organic and inorganic fertilization on yield and quality of processing tomato (Lycopersicon esculentum Mill.). Folia Hortic. 2018, 30, 321333. [Google Scholar] [CrossRef] [Green Version]
  4. Godfray, H.C.J.; Beddington, J.R.; Crute, I.R.; Haddad, L.; Lawrence, D.; Muir, J.F.; Pretty, J.; Robinson, S.; Thomas, S.M.; Toulmin, C. Food security: The challenge of feeding 9 billion people. Science 2010, 327, 812–818. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  5. Ciais, P.; Reichstein, M.; Viovy, N.; Granier, A.; Ogée, J.; Allard, V.; Aubinet, M.; Buchmann, N.; Bernhofer, C.; Carrara, A.; et al. Europewide reduction in primary productivity caused by the heat and drought in 2003. Nature 2005, 437, 529–553. [Google Scholar] [CrossRef] [PubMed]
  6. Fracasso, A.; Telò, L.; Lanfranco, L.; Bonfante, P.; Amaducci, S. Physiological beneficial effect of Rhizophagus intraradices inoculation on tomato plant yield under water deficit conditions. Agronomy 2020, 10, 71. [Google Scholar] [CrossRef] [Green Version]
  7. Campbell, B.M.; Kinyangi, J.; Nersisyan, A.; Leigh, R.A.; DibbLeigh, J.A.; Zougmoré, R.B.; Seré, S.; Aggarwal, P.K.; Hoefner, P. Perspectives: Legislating change. Nature 2013, 501, S12–S14. [Google Scholar]
  8. Eisenstein, M. Plant breeding: Discovery in a dry spell. Nature 2013, 501, S7–S9. [Google Scholar] [CrossRef]
  9. Balliu, A.; Sallaku, G.; Rewald, B. AMF inoculation enhances growth and improves the nutrient uptake rates of transplanted, saltstressed tomato seedlings. Sustainability 2015, 7, 15967–15981. [Google Scholar] [CrossRef] [Green Version]
  10. Chialva, M.; Salvioli di Fossalunga, A.; Daghino, S.; Ghignone, S.; Bagnaresi, P.; Chiapello, M.; Novero, M.; Spadaro, D.; Perotto, S.; Bonfante, P. Native soils with their microbiotas elicit a state of alert in tomato plants. New Phytol. 2018, 220, 1296–1308. [Google Scholar] [CrossRef] [Green Version]
  11. Ezawa, T.; Saito, K. How do arbuscular mycorrhizal fungi handle phosphate? New insight into finetuning of phosphate metabolism. New Phytol. 2018, 220, 1116–1121. [Google Scholar] [CrossRef] [Green Version]
  12. Lanfranco, L.; Fiorilli, V.; Gutjahr, C. Partner communication and role of nutrients in the arbuscular mycorrhizal symbiosis. New Phytol. 2018, 220, 1031–1046. [Google Scholar] [CrossRef]
  13. Subramanian, K.S.; Santhanakrishnan, P.; Balasubramanian, P. Responses of field grown tomato plants to arbuscular mycorrhizal fungal colonization under varying intensities of drought stress. Sci. Hortic. 2006, 107, 245–253. [Google Scholar] [CrossRef]
  14. Rapparini, F.; Penuelas, J. Mycorrhizal fungi to alleviate drought stress on plant growth. In Use of Microbes for the Alleviation of Soil Stresses; Miransari, M., Ed.; Springer: New York, NY, USA, 2014; Volume 1. [Google Scholar]
  15. Rouphael, Y.; Franken, P.; Schneider, C.; Schwarz, D.; Giovannetti, M.; Agnolucci, M.; De Pascale, S.; Bonini, P.; Colla, G. Arbuscular mycorrhizal fungi act as biostimulants in horticultural crops. Sci. Hortic. 2015, 196, 91–108. [Google Scholar] [CrossRef]
  16. Chitarra, W.; Pagliarani, C.; Maserti, B.; Lumini, E.; Siciliano, I.; Cascone, P.; Schubert, A.; Gambino, G.; Balestrini, R.; Guerrieri, E. Insights on the impact of arbuscular mycorrhizal symbiosis on tomato tolerance to water stress. Plant Physiol. 2016, 171, 1009–1023. [Google Scholar] [CrossRef] [Green Version]
  17. Begum, N.; Ahanger, M.A.; Su, Y.; Lei, Y.; Mustafa, N.S.A.; Ahmad, P.; Zhang, L. Improved drought tolerance by AMF inoculation in maize (Zea mays) involves physiological and biochemical implications. Plants 2019, 8, 579. [Google Scholar] [CrossRef] [Green Version]
  18. Fiorilli, V.; Maghrebi, M.; Novero, M.; Votta, C.; Mazzarella, T.; Buffoni, B.; Astolfi, S.; Vigani, G. Arbuscular mycorrhizal symbiosis differentially affects the nutritional status of two durum wheat genotypes under drought conditions. Plants 2022, 11, 804. [Google Scholar] [CrossRef]
  19. Wang, B.; Yao, Z.; Zhao, S.; Guo, K.; Sun, J.; Zhang, H. Arbuscular mycorrhizal fungal application to improve growth and tolerance of processing tomato (Lycopersicum esculentum Miller) under drought stress. J. Food Agric. Environ. 2014, 12, 452–457. [Google Scholar]
  20. Giananazzi, S.; Schuepp, H.; Barea, J.M.; Haselwandter, K. Mycorrhizal Technology in Agriculture: From Genes to Bioproducts; Birkhauser: Basel, Switzerland, 2001; p. 296. [Google Scholar]
  21. Leal, R.S. The use of Confidor S in the float, a new tobacco seedling production system in the south of Brazil. PflanzenschutzNachr. Bayer 2001, 54, 337–352. [Google Scholar]
  22. Rideout, J.W.; Overstreet, L.F. Phosphorus rate in combination with cultural practices reduces excessive growth of tomato seedlings in the float system. HortScience 2003, 38, 524–528. [Google Scholar] [CrossRef]
  23. Kakabouki, I.; Mavroeidis, A.; Tataridas, A.; Kousta, A.; Efthimiadou, A.; Karydogianni, S.; Katsenios, N.; Roussis, I.; Papastylianou, P. Effect of Rhizophagus irregularis on growth and quality of Cannabis sativa seedlings. Plants 2021, 10, 1333. [Google Scholar] [CrossRef]
  24. Roberto, K. Howto Hydroponics, 4th ed.; The Futuregarden Press: Farmingdale, NY, USA, 2003; p. 23. [Google Scholar]
  25. Akoumianaki Ioannidou, A.; Rasouli, M.; Podaropoulou, L.; Bilalis, D. Seedlings production of Mentha × piperita (peppermint) and Mentha spicata (spearmint) in float system with organic and inorganic fertilization. Acta Hortic. 2012, 937, 1307–1311. [Google Scholar] [CrossRef]
  26. Bilalis, D.; Kanatas, P.; Patsiali, S.; Konstantas, A.; Akoumianakis, K. Comparison between conventional and organic floating systems for lettuce and tomato (Lactuca sativa and Lycopersicon esculentum) seedling production. J. Food Agric. Environ. 2009, 7, 623628. [Google Scholar]
  27. Kanatas, P. Float system and crucial points of the method for seedling production and crop cultivation with or without organic fertilization. Agron. Res. 2020, 18, 137–147. [Google Scholar]
  28. Gregory, P.J. Plant Roots: Growth, Activity and Interactions with the Soil; Blackwell Publishing: Oxford, UK, 2008; pp. 108–109. [Google Scholar]
  29. Akoumianaki Ioannidou, A.; Podaropoulou, L.; Rasouli, M.; Bilalis, D. Seedlings production of Ocimum basilicum in two systems (float and seedbed) with organic and inorganic fertilization. Acta Hortic. 2012, 937, 1301–1306. [Google Scholar] [CrossRef]
  30. Bantis, F.; Dangitsis, C.; Koukounaras, A. Influence of Light Spectra from LEDs and Scion × Rootstock Genotype Combinations on the Quality of Grafted Watermelon Seedlings. Plants 2021, 10, 353. [Google Scholar] [CrossRef]
  31. Dodd, J.C.; Boddington, C.L.; Rodríguez, A.; GonzalezChavez, C.; Mansur, I. Mycelium of Arbuscular Mycorrhizal fungi (AMF) from different genera: Form, function and detection. Plant Soil 2000, 226, 131–151. [Google Scholar] [CrossRef]
  32. Ibiang, S.R.; Sakamoto, K.; Kuwahara, N. Performance of tomato and lettuce to arbuscular mycorrhizal fungi and Penicillium pinophilum EU0013 inoculation varies with soil, culture media of inoculum, and fungal consortium composition. Rhizosphere 2020, 16, 100246. [Google Scholar] [CrossRef]
  33. Jamiołkowska, A.; Thanoon, A.H.; Skwarylo, B.; Patkowska, E.; Mielniczuk, E. Mycorrhizal inoculation as an alternative for the ecological production of tomato (Lycopersicon esculentum Mill.). Int. Agrophys. 2020, 34, 253–264. [Google Scholar] [CrossRef]
  34. Dickson, A.; Leaf, A.L.; Hosner, J.F. Quality appraisal of white spruce and white pine seedling stock in nurseries. For. Chron. 1960, 36, 1013. [Google Scholar] [CrossRef]
  35. Giovannetti, M.; Mosse, B. An evaluation of techniques for measuring vesicular arbuscular mycorrhizal infection in roots. New Phytol. 1980, 84, 489–500. [Google Scholar] [CrossRef]
  36. Phillips, J.M.; Hayman, D.S. Improved procedures for clearing roots and staining parasitic and vesicular arbuscular mycorrhizal fungi for rapid assessment of infection. Trans. Br. Mycol. Soc. 1970, 55, 158–161. [Google Scholar] [CrossRef]
  37. Latef, A.A.H.A.; Hashem, A.; Rasool, S.; Abd–Allah, E.F.; Alqarawi, A.A.; Egamberdieva, D.; Jan, S.; Anjum, N.A.; Ahmad, P. Arbuscular mycorrhizal symbiosis and abiotic stress in plants: A review. J. Plant Biol. 2016, 59, 407–426. [Google Scholar] [CrossRef]
  38. Begum, N.; Qin, C.; Ahanger, M.A.; Raza, S.; Khan, M.I.; Ashraf, M.; Ahmed, N.; Zhang, L. Role of arbuscular mycorrhizal fungi in plant growth regulation: Implications in abiotic stress tolerance. Front. Plant Sci. 2019, 10, 1068. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  39. He, F.; Sheng, M.; Tang, M. Effects of Rhizophagus irregularis on photosynthesis and antioxidative enzymatic system in Robinia pseudoacacia L. under drought stress. Front. Plant Sci. 2017, 8, 183. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  40. Ortiz, N.; Armada, E.; Duque, E.; Roldán, A.; Azcón, R. Contribution of arbuscular mycorrhizal fungi and/or bacteria to enhancing plant drought tolerance under natural soil conditions: Effectiveness of autochthonous or allochthonous strains. J. Plant Physiol. 2015, 174, 87–96. [Google Scholar] [CrossRef]
  41. Wang, C.; Li, X.; Zhon, J.; Wang, G.; Dong, Y. Effects of AM fungi on the growth and yield of cucumber plants. Commun. Soil Sci. Plant Anal. 2008, 39, 499–509. [Google Scholar] [CrossRef]
  42. Nacoon, S.; Ekprasert, J.; Riddech, N.; Mongkolthanaruk, W.; Jogloy, S.; Vorasoot, N.; Cooper, J.; Boonlue, S. Growth enhancement of sunchoke by arbuscular mycorrhizal fungi under drought condition. Rhizosphere 2021, 17, 100308. [Google Scholar] [CrossRef]
  43. Nannipieri, P.; Giagnoni, L.; Landi, L.; Renella, G. Role of phosphatase enzymes in soil. In Phosphorus in Action; Bünemann, E., Oberson, A., Frossard, E., Eds.; Soil Biology; Springer: Berlin/Heidelberg, Germany, 2011; Volume 26, pp. 215–243. [Google Scholar]
  44. White, P.J.; Hammond, J.P. Phosphorus nutrition of terrestrial plants. In The Ecophysiology of Plant Phosphorus Interactions, 1st ed.; White, P.J., Hammond, J.P., Eds.; Springer: Dordrecht, The Netherlands, 2008; Volume 7, pp. 51–81. [Google Scholar]
  45. Hawkesford, M.; Horst, W.; Kichey, T.; Lambers, H.; Schjoerring, J.; Møller, I.S.; White, P. Functions of macronutrients. In Marschner’s Mineral Nutrition of Higher Plants, 3rd ed.; Marschner, P., Ed.; Elsevier Inc.: Amsterdam, The Netherlands, 2011; pp. 135–189. [Google Scholar]
  46. Jin, H.; Pfeffer, P.E.; Douds, D.D.; Piotrowski, E.; Lammers, P.J.; Shachar Hill, Y. The uptake, metabolism, transport and transfer of nitrogen in an arbuscular mycorrhizal symbiosis. New Phytol. 2005, 168, 687–696. [Google Scholar] [CrossRef]
  47. Tanaka, Y.; Yano, Y. Nitrogen delivery to maize via mycorrhizal hyphae depends on the form of N supplied. Plant Cell Environ. 2005, 28, 1247–1254. [Google Scholar] [CrossRef]
  48. Ahanger, M.A.; Tyagi, S.R.; Wani, M.R.; Ahmad, P. Drought tolerance: Role of organic osmolytes, growth regulators, and mineral nutrients. In Physiological Mechanisms and Adaptation Strategies in Plants under Changing Environment; Ahmad, P., Wani, M.R., Eds.; Springer: New York, NY, USA, 2014; Volume 1, pp. 125–155. [Google Scholar]
  49. Hameed, A.; Dilfuza, E.; Abd_Allah, E.F.; Hashem, A.; Kumar, A.; Ahmad, P. Salinity stress and arbuscular mycorrhizal symbiosis in plants. In Use of Microbes for the Alleviation of Soil Stresses; Miransari, M., Ed.; Springer Science + Business Media: New York, NY, USA, 2014; Volume 1, pp. 139–159. [Google Scholar]
  50. Hashem, A.; Alqarawi, A.A.; Radhakrishnan, R.; AlArjani, A.F.; Aldehaish, H.A.; Egamberdieva, D.; Abd_Allah, E.F. Arbuscular mycorrhizal fungi regulate the oxidative system, hormones and ionic equilibrium to trigger salt stress tolerance in Cucumis sativus L. Saudi J. Biol. Sci. 2018, 25, 1102–1114. [Google Scholar] [CrossRef]
  51. De Andrade, S.A.L.; Domingues, A.P.; Mazzafera, P. Photosynthesis is induced in rice plants that associate with arbuscular mycorrhizal fungi and are grown under arsenate and arsenite stress. Chemosphere 2015, 134, 141–149. [Google Scholar] [CrossRef]
  52. Herold, A.; Walker, D.A. Transport across Chloroplast Envelopes the Role of Phosphate. In Transport Across Single Biological Membranes, 1st ed.; Tosteson, D.C., Ed.; Springer: Berlin, Germany, 1979; Volume 2, pp. 411–439. [Google Scholar]
  53. Nemec, S.; Vu, J.C.V. Effects of soil phosphorus and Glomus Intraradices on growth, nonstructural carbohydrates, and photosynthetic activity of Citrus aurantium. Plant Soil 1990, 128, 257–263. [Google Scholar] [CrossRef]
  54. Andrino, A.; Guggenberger, G.; Kernchen, S.; Mikutta, R.; Sauheitl, L.; Boy, J. Production of organic acids by arbuscular mycorrhizal fungi and their contribution in the mobilization of phosphorus bound to iron oxides. Front. Plant Sci. 2021, 12, 661842. [Google Scholar] [CrossRef]
  55. Al Arjani, A.B.F.; Hashem, A.; Abd_Allah, E.F. Arbuscular mycorrhizal fungi modulate dynamics tolerance expression to mitigate drought stress in Ephedra foliata Boiss. Saudi J. Biol. Sci. 2020, 27, 380–394. [Google Scholar] [CrossRef]
  56. López Ráez, J.A.; Verhage, A.; Fernández, I.; García, J.M.; Azcón Aguilar, C.; Flors, V.; Pozo, M.J. Hormonal and transcriptional profiles highlight common and differential host responses to arbuscular mycorrhizal fungi and the regulation of the oxylipin pathway. J. Exp. Bot. 2010, 61, 2589–2601. [Google Scholar] [CrossRef] [Green Version]
  57. Vlot, A.C.; Dempsey, D.A.; Klessig, D.F. Salicylic acid, a multifaceted hormone to combat disease. Annu. Rev. Phytopathol. 2009, 47, 177–206. [Google Scholar] [CrossRef] [Green Version]
  58. Bolandnazar, S.; Neyshabouri, M.R.; Aliasgharzad, N.; Chaparzadeh, N. Effects of mycorrhizal colonization on growth parameters of onion under different irrigation and soil conditions. Pak. J. Biol. Sci. 2007, 10, 1491–1495. [Google Scholar]
  59. Krishna, H.; Singh, S.K.; Minakshi; Patel, V.B.; Khawale, R.N.; Deshmukh, P.S.; Jindal, P.C. Arbuscular mycorrhizal fungi alleviate transplantation shock in micropropagated grapevine (Vitis vinifera L.). J. Hortic. Sci. Biotechnol. 2006, 81, 259–263. [Google Scholar] [CrossRef]
  60. Ruiz Lozano, J.M. Arbuscular mycorrhizal symbiosis and alleviation of osmotic stress. New perspectives for molecular studies. Mycorrhiza 2003, 13, 309–317. [Google Scholar] [CrossRef]
  61. Kishor, P.B.K.; Kumari, P.H.; Sunita, M.S.L.; Sreenivasulu, N. Role of proline in cell wall synthesis and plant development and its implications in plant ontogeny. Front. Plant Sci. 2015, 6, 544. [Google Scholar] [CrossRef] [Green Version]
  62. Castillo, C.R.; Sotomayor, L.S.; Ortiz, C.O.; Leonelli, G.C.; Borie, F.B.; Rubio, R.H. Effect of arbuscular mycorrhizal fungi on an ecological crop of chili peppers (Capsicum annum L.). Chilean J. Agric. Res. 2009, 69, 79–87. [Google Scholar] [CrossRef]
  63. Balota, E.L.; Machineski, O.; Truber, P.V.; Scherer, A.; De Souza, F.S. Physic nut plants present high mycorrhizal dependency under conditions of low phosphate availability. Braz. J. Plant Physiol. 2011, 23, 33–44. [Google Scholar] [CrossRef]
  64. Carmo, É.R.D.; Da Silva, C.F.; Freitas, M.S.M.; Lima, K.B.; Martins, M.A. Production of Australian cedar seedlings inoculated with arbuscular mycorrhizal fungi in different types of containers. Rev. Árvore 2016, 40, 269–278. [Google Scholar] [CrossRef] [Green Version]
  65. Aguilar, E.E.Q.; Montoya Martínez, A.C.; Rincón Enriquez, G.; Lobit, P.; López Pérez, L. Effectiveness of native arbuscular mycorrhizal consortia on the growth of Agave inaequidens. J. Soil Sci. Plant Nutr. 2016, 16, 1052–1064. [Google Scholar]
  66. Almeida, U.O.; Carvalho Andrade Neto, R.; Pereira Lunz, A.M.; Nogueira, S.R.; Costa, D.A.; Araújo, J.M. Environment and slow-release fertilizer in the production of Euterpe precatoria seedlings. Pesq. Agropec. Trop. 2018, 48, 382–389. [Google Scholar] [CrossRef]
Sustainability 14 09001 g001 550
Figure 1. Percentage of arbuscular mycorrhizal fungi (AMF) colonization of processing tomato roots as affected by the different treatments of AM fungus Rhizophagus irregularis measured at 5, 9, 13, 17, 21 and 25 days after emergence (DAE). Vertical lines represent standard mean errors. The different lowercase letters in the values of different AMF treatments for each time point of measurement denote statistically significant differences according to the Tukey’s HSD test (p ≤ 0.05).
Figure 1. Percentage of arbuscular mycorrhizal fungi (AMF) colonization of processing tomato roots as affected by the different treatments of AM fungus Rhizophagus irregularis measured at 5, 9, 13, 17, 21 and 25 days after emergence (DAE). Vertical lines represent standard mean errors. The different lowercase letters in the values of different AMF treatments for each time point of measurement denote statistically significant differences according to the Tukey’s HSD test (p ≤ 0.05).
Sustainability 14 09001 g001
Table
Table 1. Experimental treatments and total AM fungus Rhizophagus irregularis applied rates.
Table 1. Experimental treatments and total AM fungus Rhizophagus irregularis applied rates.
TreatmentMycoPlant® Polvo Grow Dose
(g per L of Nutrient Solution)		Applied Fungal Spores per L of Nutrient SolutionTotal Applied
Fungal Spores in Nutrient Solution of Each Trough
Control---
AMF10.1402000
AMF20.2804000
AMF30.31206000
Table
Table 2. Chemical composition of organic water-soluble fertilizer Fish-Fert.
Table 2. Chemical composition of organic water-soluble fertilizer Fish-Fert.
Chemical CharacteristicsValues
pH6.70 ± 0.20
Nitrogen (N % w/w)2.00 ± 0.10
Phosphorus (P2O5 % w/w)4.00 ± 0.02
Potassium (K2O % w/w)0.20 ± 0.02
Calcium (CaO % w/w)0.60 ± 0.04
Magnesium (MgO % w/w)0.09 ± 0.01
Sulphur (S %)0.10 ± 0.02
Iron (Fe mg kg−1)26.0 ± 1.05
Copper (Cu mg kg−1)1.0 ± 0.08
Zinc (Zn mg kg−1)13.0 ± 0.05
Manganese (Mn mg kg−1)3.0 ± 0.03
Amino acids (% w/w)55.00 ± 1.80
Table
Table 3. Biometric characteristics of processing tomato seedlings as affected by the different treatments of AM fungus Rhizophagus irregularis.
Table 3. Biometric characteristics of processing tomato seedlings as affected by the different treatments of AM fungus Rhizophagus irregularis.
Total Root Length (cm)Root Dry Weight (g)Shoot Length (cm)Stem
Diameter (cm)		Shoot Dry Weight (g)Root/Shoot RatioSeedling Total Dry Weight (g)
Control22.84 c0.179 c7.89 a2.69 a0.675 b0.267 a0.855 b
AMF128.88 b0.207 bc7.94 a2.73 a0.892 ab0.233 a1.097 ab
AMF232.31 ab0.251 ab8.13 a2.71 a0.956 ab0.264 a1.206 ab
AMF335.34 a0.276 a8.22 a2.78 a1.113 a0.248 a1.386 a
FAMF12.289 *13.712 *2.293 ns1.224 ns11.570 *1.993 ns12.808 *
F–test ratios are from ANOVA. ns and *: Not significant and significant at 5% probability level, respectively. The different lowercase letters within a column denote statistically significant differences according to the Tukey’s HSD test (p ≤ 0.05).
Table
Table 4. Dickson’s quality index (DQI), survival rate, and nitrogen (N) and phosphorus (P) content of processing tomato seedlings as affected by the different treatments of AM fungus Rhizophagus irregularis.
Table 4. Dickson’s quality index (DQI), survival rate, and nitrogen (N) and phosphorus (P) content of processing tomato seedlings as affected by the different treatments of AM fungus Rhizophagus irregularis.
Dickson’s Quality
Index (DQI)		N Content
(mg 100 g−1 DW)		P Content
(mg 100 g−1 DW)		Survival Rate (%)
Control0.128 c2.714 c0.373 c89.87 b
AMF10.152 bc2.883 bc0.434 b90.91 b
AMF20.177 ab3.165 ab0.463 ab93.74 a
AMF30.198 a3.376 a0.497 a94.78 a
FAMF16.034 *21.189 **20.828 **32.307 **
F–test ratios are from ANOVA. * and **: Significant at 5% and 1% probability levels, respectively. The different lowercase letters within a column denote statistically significant differences according to the Tukey’s HSD test (p ≤ 0.05).
Table
Table 5. Correlation matrix among evaluated traits.
Table 5. Correlation matrix among evaluated traits.
TraitCoefficient of Correlation (r)
AMF
Colonization
25 DAE		Total Root LengthRoot Dry WeightShoot LengthStem
Diameter		Shoot Dry WeightRoot/Shoot RatioSeedling Total Dry WeightDickson’s Quality Index (DQI)N ContentP Content
Total Root Length0.9590 ***
Root Dry Weight0.8916 **0.9588 ***
Shoot Length0.7287 *0.8881 **0.9226 **
Stem Diameter0.5631 ns0.5666 ns0.5312 ns0.4831 ns
Shoot Dry Weight0.8995 **0.9143 **0.9358 ***0.7916 *0.6598 ns
Root/Shoot Ratio–0.2465 ns–0.1209 ns–0.0622 ns0.1319 ns–0.5313 ns–0.4068 ns
Seedling Total Dry Weight0.9071 **0.9322 ***0.9577 ***0.8249 *0.6416 ns0.9977 ***0.3442 ns
Dickson’s quality index (DQI)0.9080 **0.9558 ***0.9917 ***0.8877 **0.6036 ns0.9717 ***0.1846 ns0.9854 ***
N content0.9077 **0.8946 **0.9028 **0.7412 *0.5585 ns0.8581 **0.0716 ns0.8754 **0.9084 **
P content0.9239 **0.8816 **0.9061 **0.6880 ns0.5493 ns0.9595 ***0.3692 ns0.9589 ***0.9381 ***0.8680 **
Survival Rate0.8672 **0.9053 **0.9702 ***0.8369 **0.5549 ns0.9189 **0.0849 ns0.9381 ***0.9711 ***0.9474 ***0.9136 **
ns, *, ** and ***: Not significant and significant at 5%, 1% and 0.1% probability levels, respectively.
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Share and Cite

MDPI and ACS Style

Roussis, I.; Beslemes, D.; Kosma, C.; Triantafyllidis, V.; Zotos, A.; Tigka, E.; Mavroeidis, A.; Karydogianni, S.; Kouneli, V.; Travlos, I.; et al. The Influence of Arbuscular Mycorrhizal Fungus Rhizophagus irregularis on the Growth and Quality of Processing Tomato (Lycopersicon esculentum Mill.) Seedlings. Sustainability 2022, 14, 9001. https://doi.org/10.3390/su14159001

AMA Style

Roussis I, Beslemes D, Kosma C, Triantafyllidis V, Zotos A, Tigka E, Mavroeidis A, Karydogianni S, Kouneli V, Travlos I, et al. The Influence of Arbuscular Mycorrhizal Fungus Rhizophagus irregularis on the Growth and Quality of Processing Tomato (Lycopersicon esculentum Mill.) Seedlings. Sustainability. 2022; 14(15):9001. https://doi.org/10.3390/su14159001

Chicago/Turabian Style

Roussis, Ioannis, Dimitrios Beslemes, Chariklia Kosma, Vassilios Triantafyllidis, Anastasios Zotos, Evangelia Tigka, Antonios Mavroeidis, Stella Karydogianni, Varvara Kouneli, Ilias Travlos, and et al. 2022. "The Influence of Arbuscular Mycorrhizal Fungus Rhizophagus irregularis on the Growth and Quality of Processing Tomato (Lycopersicon esculentum Mill.) Seedlings" Sustainability 14, no. 15: 9001. https://doi.org/10.3390/su14159001

APA Style

Roussis, I., Beslemes, D., Kosma, C., Triantafyllidis, V., Zotos, A., Tigka, E., Mavroeidis, A., Karydogianni, S., Kouneli, V., Travlos, I., & Kakabouki, I. (2022). The Influence of Arbuscular Mycorrhizal Fungus Rhizophagus irregularis on the Growth and Quality of Processing Tomato (Lycopersicon esculentum Mill.) Seedlings. Sustainability, 14(15), 9001. https://doi.org/10.3390/su14159001

Note that from the first issue of 2016, this journal uses article numbers instead of page numbers. See further details here.

Article Metrics

Back to TopTop