Next Article in Journal
Antioxidant, Enzyme Inhibitory, and Protective Effect of Amelanchier lamarckii Extract
Previous Article in Journal
Effects of Lactone- and Ketone-Brassinosteroids of the 28-Homobrassinolide Series on Barley Plants under Water Deficit
 
 
Search for Articles:
Title / Keyword
Author / Affiliation / Email
Journal
Article Type
 
 
Advanced Search
 
Section
Special Issue
Volume
Issue
Number
Page
 
Journals
Plants
Volume 13
Issue 10
10.3390/plants13101346
plants-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

How Rhizosphere Microbial Assemblage Is Influenced by Dragon Fruits with White and Red Flesh

by
Xinyan Zhou
1,
Siyu Chen
1,
Lulu Qiu
1,
Liyuan Liao
1,
Guifeng Lu
2,* and
Shangdong Yang
1,*
1
Guangxi Key Laboratory of Agro-Environment and Agro-Products Safety, National Demonstration Center for Experimental Plant Science Education, Agricultural College, Guangxi University, Nanning 530004, China
2
Horticulture Research Institute, Guangxi Academy of Agricultural Sciences, Nanning 530007, China
*
Authors to whom correspondence should be addressed.
Plants 2024, 13(10), 1346; https://doi.org/10.3390/plants13101346
Submission received: 5 April 2024 / Revised: 5 May 2024 / Accepted: 11 May 2024 / Published: 13 May 2024
(This article belongs to the Special Issue Plant-Soil Microbe Interactions in Ecosystems)
Browse Figures
Review Reports Versions Notes

Abstract

:
The synthesis of betalain using microorganisms is an innovative developmental technology, and the excavation of microorganisms closely related to betalain can provide certain theoretical and technical support to this technology. In this study, the characteristics of soil microbial community structures and their functions in the rhizospheres of white-fleshed dragon fruit (Hylocereus undatus) and red-fleshed dragon fruit (Hylocereus polyrhizus) were analyzed. The results show that the soil bacterial and fungal compositions in the rhizospheres were shaped differently between H. undatus and H. polyrhizus. Bacterial genera such as Kribbella and TM7a were the unique dominant soil bacterial genera in the rhizospheres of H. undatus, whereas Bradyrhizobium was the unique dominant soil bacterial genus in the rhizospheres of H. polyrhizus. Additionally, Myrothecium was the unique dominant soil fungal genus in the rhizospheres of H. polyrhizus, whereas Apiotrichum and Arachniotus were the unique dominant soil fungal genera in the rhizospheres of H. undatus. Moreover, TM7a, Novibacillus, Cupriavidus, Mesorhizobium, Trechispora, Madurella, Cercophora, and Polyschema were significantly enriched in the rhizospheres of H. undatus, whereas Penicillium, Blastobotrys, Phialemonium, Marasmius, and Pseudogymnoascus were significantly enriched in the rhizospheres of H. polyrhizus. Furthermore, the relative abundances of Ascomycota and Penicillium were significantly higher in the rhizospheres of H. polyrhizus than in those of H. undatus.

1. Introduction

Dragon fruit can be categorized into two varieties based on the color of its flesh, distinguished as white (Hylocereus undatus) and red (Hylocereus polyrhizus) flesh [1,2]. H. polyrhizus is rich in betalain, which is a water-soluble natural plant pigment [3]. In contrast, H. undatus lacks betalain. Therefore, H. polyrhizus has an advantage over H. undatus, contributing to minerals, proteins, phenolics, and antioxidant properties [4,5,6,7]. Due to the gradual appreciation of betalain as a food additive and its potential medicinal value, based on biotechnologies, producing betalain has become a hot spot for researchers.
Rhizospheric soil microbial community composition is closely related to the plant variety [8,9], and different plant varieties produce diverse compositions by recruiting various soil microbial communities in the rhizospheres [10,11]. It has been demonstrated that the soil microbial community structure significantly differs in rhizospheres among poplar varieties [12]. Additionally, soil microbial community structures not only significantly differ in the rhizospheres of different soybean varieties but, also, each soybean variety has specific soil microbial compositions and networks in different rhizospheres [13,14]. Moreover, soil microbiomes in the rhizospheres of olives [15] and pumpkins [16,17] differ between different varieties.
Previous studies have confirmed that the rhizospheric soil microbial community interacts with plant varieties [18,19]. Firstly, the functional requirements of plants play a crucial role in the assembly of rhizospheric microbial communities [20]. Plant varieties can not only shape the soil microbial community structures in rhizospheres but also affect the soil microbial functions in rhizospheres [21]. For instance, studies have reported that soil microbial compositions and functions in the rhizospheres of strawberries significantly depend on the variety, and disease-resistant and high-yielding strawberry varieties commonly recruit more beneficial soil microbes [22]. Additionally, a mulberry variety resistant to bacterial wilt was reported to be enriched with fungal communities that can prevent the spread of soil-borne diseases, enhance plant drought resistance, and provide tolerance against biological or abiotic stresses [23]. Chen et al. [24] found that different rhizospheric soil microbes are recruited by tomatoes with different fruit color phenotypes. Xiao et al. [25] also found differences in rhizospheric microbes recruited by different watermelon phenotypes relating to rind color formation. In addition, plant traits were also significantly influenced by soil microorganisms [26], such as disease resistance [27], root architecture [28], and drought tolerance [29], all of which are modified by soil microbes in rhizospheres.
Additionally, soil microorganisms are also able to produce various phytohormones related to fruit pigment production and metabolite accumulation, some of which are also closely related to the synthesis of betalain [30]; for example, cyanobacteria serve as the favored origin of exogenous cytokinin [31]. These cytokinins play a crucial role in enhancing the accumulation of betalain by activating the dopa oxidase protein and binding it to tyrosine [32]. Botrytis fungi can produce abscisic acid [33], Aspergillus fungi can synthesize gibberellins [34], and abscisic acid and gibberellins inhibit betalain biosynthesis [35]. B. rhodina has the potential to produce jasmonate under controlled conditions [36]. Jasmonate can be induced by ultraviolet-B irradiation and can promote betalain accumulation [37]. Additionally, the biosynthesis pathways of betalain were found to be associated with Streptomyces, Bacillus megaterium, Agaricus bisporus, and Hygrocybe [38,39,40,41]. Research on the synthesis of betalain using microorganisms has also been developed. For example, Grewal et al. [42] achieved the microbial synthesis of betalain from glucose using Saccharomyces cerevisiae; Wang et al. [43] used biofilm surface fermentation to produce betalain from Penicillium novae-zelandiae. The fruits of red-fleshed dragon fruit (H. polyrhizus) contain abundant betalain, but whether soil microbes in rhizospheres contribute to betalain synthesis is unknown, as, to date, there are no reports on this. Therefore, the differences in soil microbial compositions in the rhizospheres of white-fleshed dragon fruit (H. undatus) and red-fleshed dragon fruit (H. polyrhizus) were analyzed.

2. Materials and Methods

2.1. Experimental Site

This experiment was conducted at the vegetable base of the Agricultural College, Guangxi University, Nanning, Guangxi, P.R. China (108°17′25″ E, 22°51′02″ N). Twenty-five plants each of the varieties ‘Nanning white-flesh’ (H. undatus, RW) and ‘YuanzhiHong red-flesh’ (H. polyrhizus, RR) (Figure 1) were planted in pots (40 cm high and 35 cm in diameter) in October 2021, one plant in each pot.
The soil physicochemical properties were as follows: soil pH 5.84; organic matter content 9.46 g·kg−1; total nitrogen, phosphorus, and potassium 0.62 g·kg−1, 0.76 g·kg−1, and 7.83 g·kg−1, respectively. The available nitrogen, phosphorus, and potassium contents were 16.36 mg·kg−1, 0.56 mg·kg−1, and 86.35 mg·kg−1, respectively.

2.2. Soil Sample Collection

The samples were collected in July 2022. Rhizospheric soil samples were collected using the shaking-off method. Briefly, three dragon fruit plants of each variety were randomly selected and loosened to approximately 25 cm in diameter using a sterile shovel, after which the base of each plant was pulled up entirely with the soil. The soil adhering to the dragon fruit roots was carefully collected as the rhizospheric soil in a sterile bag. Soil samples were also collected from the same field without any plant growth treatment as background soil (CK) and then transported to the laboratory as quickly as possible. After the samples were passed through a 2 mm stainless-steel sieve, the sifted soil was stored at −80 °C.

2.3. Test Methods

Total DNA extraction and polymerase chain reaction (PCR) amplification of the plant rhizosphere samples were conducted as follows: Total DNA extraction was performed according to the instructions of the Fast DNA® Spin Kit for Soil (MP Biomedicals, Thomas Irvine, CA, USA), and the DNA concentration and purity were determined using a NanoDrop 2000 spectrophotometer (Thermo Fisher Scientific, Waltham, MA, USA). The extracted DNA was examined on a 1% agarose gel, the quality of the extracted DNA was detected via gel electrophoresis, and PCR amplification was performed on an GeneAmp® 9700 (ABI, Los Angeles, CA, USA) using the extracted rhizosphere microbial DNA as a template.
Illumina MiSeq sequencing was performed as follows: PCR products from the same sample were recovered using a gel recovery kit, purified by elution with Tris-HCl buffer, and then recovered using a 2% agarose gel for detection and quantification of the recovered products using a Quantus™ Fluorometer (Promega, Madison, MI, USA). Illumina library construction was performed using purified amplified fragments. Sequencing was performed using Illumina’s MiSeq PE platform. The bacterial 16S rRNA gene was amplified using the primer pair 338F (5′-ACTCCTACGGGAGGCAGCAG-3′) and 806R (5′-GGACTACHVGGGTWTCTAAT-3′). For the amplification of fungal ITS regions, the primer pair ITS1F (5′-CTTGGTCATTTAGAGGAAGTAA-3′) and ITS2R (5′-GCTGCGTTCTTCATCGATGC-3′) was employed. The raw data for soil bacterial and fungal sequences were deposited in the NCBI Sequence Read Archive (SRA) database under accession numbers PRJNA1066732 and PRJNA1066751, respectively.
The paired-end (PE) reads obtained from Illumina sequencing were first spliced according to the overlap relationship, while the sequences were quality-controlled and filtered, and the samples were differentiated and then analyzed through clustering and species taxonomy using the I-sanger cloud data analysis platform (http://www.majorbio.com) of the Majorbio Bio-Pharm Technology Co., Ltd. (Shanghai, China). Based on the taxonomic information, statistical analysis of the community structure was performed at each taxonomic level. The operational taxonomic unit (OTU) clustering steps were as follows: Utilizing Uparse software (version 7.0.1), non-redundant sequences were extracted from optimized sequences to facilitate a reduction in the redundant computational burden in the intermediate analysis processes. The non-redundant sequences (excluding single sequences) were clustered into OTUs based on 97% similarity, and chimeras were removed during the clustering process to obtain representative sequences of the OTUs. Subsequently, all optimized sequences were mapped to the representative sequences of the OTUs, and sequences with a similarity of 97% or higher to the OTU representative sequences were selected to generate the OTU table. Taxonomic analysis of representative sequences of OTUs at a 97% similarity level was conducted using the RDP Classifier version 2.11 on the QIIME platform (http://qiime.org/scripts/assign_taxonomy.html, accessed on 17 March 2023). A confidence threshold of 0.7 was applied to obtain species classification information corresponding to each OTU. Bacteria and fungi were individually aligned against the Silva database (Release 138, http://www.arb-silva.de) and the Unite database (Release 8.0, http://unite.ut.ee/index.php, accessed on 17 March 2023) for comparative analysis.

2.4. Statistical Analysis

The experimental data underwent statistical analysis using Excel 2019 and SPSS Statistics 18 software. Data are presented as the mean ± standard deviation (SD). The analysis of the rhizosphere microbial community structure encompassed alpha diversity analysis of bacteria and fungi, so we utilized the Shannon and Invsimpson indices to estimate the microbial diversity, and the Ace and Chao indices were used to represent species richness. Additionally, we conducted taxonomic analyses at the phylum and genus levels for rhizosphere microbial communities, exploring distinctions between the rhizosphere microbial community structures of H. undatus and H. polyrhizus.

3. Results

3.1. Soil Microbial Diversity in the Rhizospheres of Dragon Fruits with White and Red Flesh

As shown in Table 1, the coverage indices reached at least 98%, indicating that the results may effectively reflect the true situation of the species. The soil bacterial diversity indices, i.e., the Shannon and Invsimpson indices, were not significantly different in the rhizospheres of the two dragon fruits with white and red flesh and neither were the soil bacterial richness indices, i.e., the Ace and Chao indices. Moreover, the soil fungal diversity and richness in the rhizospheres between the two dragon fruits with white and red flesh also displayed the same trends as those of the soil bacterial community.
Principal coordinates analysis (PCoA) based on the OTU level (Bray–Curtis distance, Adonis test) revealed that, for soil bacteria in RW, RR, and CK, the Adonis test results were R2 = 0.3785, p = 0.005 (Figure 2A); for fungi, the Adonis test results were R2 = 0.6406, p = 0.005 (Figure 2C). All of the above results indicate that the differences between treatment groups were greater than those within treatment groups. Additionally, these findings suggest that the data analysis was reliable. Meanwhile, it also indicates that there were highly significant differences (p < 0.01) in the community composition of rhizosphere bacteria and fungi among RW, RR, and CK.
Moreover, partial least squares discriminant analysis (PLS-DA) also showed that the soil bacterial (Figure 2B) and fungal (Figure 2D) compositions at the OTU level clustered separately in RW, RR, and CK. Furthermore, based on the dispersion of the sample point distributions, each group of samples clustered together with relatively little variation in community structure within the group.
As an example, the soil microbial communities in rhizospheres of RW and RR exhibited significant differences.

3.2. Soil Microbial Community Structure in the Rhizospheres of Dragon Fruits with White and Red Flesh

As shown in Figure 3A, the common dominant endophytic bacterial phyla (the relative abundances were higher than 1%) in RW and RR were Actinobacteriota (28.95–30.83%), Pseudomonadota (25.05–26.01%), Firmicutes (12.17–9.98%), Chloroflexi (10.27–11.25%), Acidobacteriota (6.27–7.16%), Gemmatimonadota (4.56–5.02%), Bacteroidota (3.91–3.43%), Patescibacteria (2.80–1.01%), and Myxococcota (2.03–1.74%) (The first value corresponds to RW and the second to RR, the same below).
The common dominant endophytic bacterial genera (the relative abundances were higher than 1%) in RW and RR were Actinomadura (3.92–4.03%), Sphingomonas (3.64–3.95%), Saccharomonospora (3.31–3.25%), Bacillus (2.09–1.71%), Novibacillus (1.78–1.37%), Gemmatimonas (1.58–1.58%), Streptomyces (1.38–1.21%), Haloactinopolyspora (1.19–1.21%), Knoellia (1.16–1.16%), and Acidibacter (1.01–1.02%) (Figure 3B).
Further, Kribbella (1.33%) and TM7a (1.11%) were the unique dominant soil bacterial genera in the rhizosphere of RW, whereas Bradyrhizobium (1.05%) was the unique dominant soil bacterial genus in the rhizosphere of RR.
In addition, the common dominant endophytic fungal phyla in RW and RR were Ascomycota (51.28–73.75%), Basidiomycota (40.33–18.10%), Mortierellomycota (2.62–3.06%), and Chytridiomycota (2.22–1.44%) (Figure 4A).
At the genus level, the common dominant endophytic fungal genera in RW and RR were Trechispora (24.93–9.54%), Trichocladium (13.30–8.35%), Saitozyma (11.55–4.27%), Penicillium (9.72–29.63%), Talaromyces (4.21–6.00%), Mortierella (2.57–2.97%), Trichoderma (2.33–2.77%), Aspergillus (2.26–4.22%), Chaetomium (1.56–2.50%), and Apiotrichum (1.10–1.49%) (Figure 4B).
Additionally, Arachniotus (1.02%) was the unique dominant soil fungal genus in the rhizosphere of RW, whereas Myrothecium (2.58%) was the unique dominant soil fungal genus in the rhizosphere of RR.
Linear discriminant analysis effect size (LEfSe) analysis with a linear discriminant analysis (LDA) threshold of 3.0 was employed to investigate the significant variances and primary influential biomarker categories between bacterial communities inhabiting the rhizosphere soils of RW and RR. A higher LDA score indicates a greater impact on species abundance under differential effects.
As shown in Figure 5, TM7a, Novibacillus, Cupriavidus, and Mesorhizobium were significantly enriched in the rhizospheres of RW.
Moreover, Trechispora, Madurella, Cercophora, and Polyschema were significantly enriched in the rhizospheres of RW, whereas Penicillium, Blastobotrys, Phialemonium, Marasmius, and Pseudogymnoascus were significantly enriched in the rhizospheres of RR (Figure 6).

3.3. Functional Prediction of Soil Microorganisms in the Rhizospheres between the Two Dragon Fruits with White and Red Flesh

Phylogenetic investigation of communities by reconstruction of unobserved states 2 (PICRUSt2) functional prediction was used to analyze the expression of the soil bacteria between RW and RR (Figure 7). The top 10 pathways were aerobic respiration Ⅰ (cytochrome c), pyruvate fermentation to isobutanol (engineered), L-isoleucine biosynthesis Ⅱ, L-isoleucine biosynthesis Ⅰ (from threonine), L-valine biosynthesis, super pathway of branched amino acid biosynthesis, fatty acid salvage, TCA cycle V (2-oxoglutarate/ferredoxin oxidoreductase), TCA cycle Ⅰ (prokaryotic), and L- isoleucine biosynthesis Ⅲ. Additionally, a Wilcoxon rank sum test was used to assess the soil bacterial expression between the rhizospheres of RW and RR. The results show that there was no significant difference in the expression of soil bacteria in each pathway between the rhizospheres of the dragon fruits with white and red flesh. However, the expression of bacteria in the rhizosphere of the 10 RR-related MetaCyc pathways was higher than that of RW.
FUNGuild software (http://www.funguild.org/, accessed on 20 March 2023) was also used to predict the functions of the soil fungal communities in the rhizospheres of RW and RR. The results show that soil fungi could be divided into three types based on their nutrition modes, i.e., Symbiotroph, Pathotroph, and Saprotroph. Furthermore, based on the fungal community pathways, fungi in the rhizospheres of RW and RR can be classified into nine guilds, i.e., Undefined Saprotroph, unknown; Fungal Parasite-Undefined Saprotroph; Animal Pathogen-Dung Saprotroph-Endophyte-Epiphyte-Plant Saprotroph-Wood Saprotroph, Wood Saprotroph, Endophyte-Litter Saprotroph-Soil Saprotroph-Undefined Saprotroph, Plant Pathogen, Animal Pathogen, Soil Saprotroph, and others. In comparison with those of soil fungi in the rhizospheres of RW, the relative abundances of soil fungi in the rhizospheres of RR associated with the Fungal Parasite-Undefined Saprotroph and Wood Saprotroph guilds decreased; however, the relative abundances of soil fungi associated with the Saprotroph guild in RR were greater than in those in RW (Figure 8).

4. Discussion

Different plant varieties have a direct impact on the soil microbial community in rhizospheres [44]. This is attributed to the fact that diverse plant roots secrete distinct substances and specific molecular signals [45,46,47]. Consequently, the compositions of soil microbes can be influenced by different plants [48], leading to the enrichment of diverse soil microbes in specific microenvironments, such as the rhizospheres of various plants [49,50,51]. In this study, we analyzed the characteristics of soil microbial community structures and their functions in the rhizospheres of white-fleshed dragon fruit (Hylocereus undatus) and red-fleshed dragon fruit (Hylocereus polyrhizus). The results indicate that the soil bacterial and fungal compositions in the rhizospheres were shaped differently between H. undatus and H. polyrhizus.
In terms of bacterial community composition, Actinobacteriota, Pseudomonadota, Firmicutes, Chloroflexi, Acidobacteriota, Gemmatimonadota, Bacteroidota, Patescibacteria, and Myxococcota were the common dominant soil bacterial phyla in the rhizospheres of H. undatus and H. polyrhizus. Kribbella and TM7a were the unique dominant bacterial genera in the rhizospheres of H. undatus, while Bradyrhizobium was found as the unique dominant genus in the rhizospheres of H. polyrhizus. The LEfSe analysis also showed that TM7a, Novibacillus, Cupriavidus, and Mesorhizobium were significantly enriched in the rhizospheres of H. undatus, contributing to the significant difference between H. undatus and H. polyrhizus.
Additionally, at the phylum level, Ascomycota had the highest relative abundance in the rhizospheres of both H. undatus and H. polyrhizus, but the relative abundance of this phylum in the rhizosphere of H. polyrhizus was 1.438 times higher than that in H. undatus. As Ascomycota is the most widely studied microbial group in terms of pigment production [52], filamentous ascomycetes fungi have been confirmed as a source of natural pigments. For instance, fungal genera such as Aspergillus and Penicillium belong to Ascomycota; they can produce natural pigments, ranging from yellow to purple [53,54,55]. Moreover, Neurospora is also considered a potential carotenoid producer but does not produce mycotoxins; Fusarium oxysporum can produce pink to purple anthranoid pigments [56]. Changes in microbial communities can be induced by plants; they can also provide feedback on plant growth [57]. Particularly, rhizospheric soil microorganisms are closely associated with plant traits [58]. As Ascomycota was abundantly enriched in the rhizospheres of H. polyrhizus, it can also be speculated that it is closely related to its betalain-rich characteristic.
Further, at the genus level, Penicillium showed the highest relative abundance of any fungal genus in rhizospheres of H. polyrhizus, and its relative abundance was 3.048 times higher than that of H. undatus. The LEfSe analysis also revealed that Penicillium, Blastobotrys, Phialemonium, Marasmius, and Pseudogymnoascus were significantly enriched in rhizospheres of H. polyrhizus. Previous studies have confirmed that orange-red to red pigments, carotenoids, and betalain could all be derived from Penicillium [43,59,60].
Plant varieties not only affect the microbial community structure but also have an impact on microbiome functions [61]. Our results also showed that the expression levels of the top 10 bacterial MetaCyc pathways in the rhizospheres of H. polyrhizus were higher than those of H. undatus. Meanwhile, higher abundances of saprophytic nutritive fungi, but lower abundances of parasitic fungi, were detected in the rhizospheres of H. polyrhizus than those of H. undatus.

5. Conclusions

Soil microbial compositions are shaped differently in the rhizospheres of dragon fruits with white (H. undatus) and red (H. polyrhizus) flesh. Although part of the shared dominant microbial genera could be detected in the rhizospheres of these two dragon fruit genotypes, Kribbella and TM7a were the unique dominant soil bacterial genera in the rhizospheres of H. undatus; in contrast, Bradyrhizobium was the unique dominant soil bacterial genus in the rhizospheres of H. polyrhizus. Additionally, Arachniotus was the unique dominant soil fungal genus in the rhizospheres of H. undatus. Myrothecium was the unique dominant soil fungal genus in the rhizospheres of H. polyrhizus.

Author Contributions

Conceptualization, X.Z. and S.Y.; methodology, S.Y.; software, X.Z. and S.C.; formal analysis, X.Z., L.Q. and L.L.; investigation, X.Z. and S.Y.; resources, G.L.; data curation, X.Z., S.C. and L.Q.; writing—original draft preparation, X.Z.; writing—review and editing, X.Z. and S.Y.; visualization, X.Z. and S.C.; project administration, S.Y.; funding acquisition, S.Y. and G.L. All authors have read and agreed to the published version of the manuscript.

Funding

This research was funded by Guangxi Key R&D Program Projects (2023AB17031).

Data Availability Statement

The raw data for soil bacterial and fungal sequencing were deposited in the NCBI Sequence Read Archive (SRA) database under accession numbers PRJNA1066732 and PRJNA1066751, respectively.

Conflicts of Interest

The authors declare no conflicts of interest.

References

  1. Arivalagan, M.; Karunakaran, G.; Roy, T.; Dinsha, M.; Sindhu, B.; Shilpashree, V.; Satisha, G.; Shivashankara, K. Biochemical and nutritional characterization of dragon fruit (Hylocereus species). Food Chem. 2021, 353, 129426. [Google Scholar] [CrossRef] [PubMed]
  2. Huang, Y.; Brennan, M.A.; Kasapis, S.; Richardson, S.J.; Brennan, C.S. Maturation Process, Nutritional Profile, Bioactivities and Utilisation in Food Products of Red Pitaya Fruits: A Review. Foods 2021, 10, 2862. [Google Scholar] [CrossRef] [PubMed]
  3. Rebecca, O.P.S.; Boyce, A.N.; Chandran, S. Ran Pigment identification and antioxidant properties of red dragon fruit (Hylocereus polyrhizus). Afr. J. Biotechnol. 2010, 9, 1450–1454. [Google Scholar] [CrossRef]
  4. Angonese, M.; Motta, G.E.; de Farias, N.S.; Molognoni, L.; Daguer, H.; Brugnerotto, P.; Costa, A.C.d.O.; Müller, C.M.O. Organic dragon fruits (Hylocereus undatus and Hylocereus polyrhizus) grown at the same edaphoclimatic conditions: Comparison of phenolic and organic acids profiles and antioxidant activities. LWT 2021, 149, 111924. [Google Scholar] [CrossRef]
  5. Nurliyana, R.; Zahir, I.S.; Suleiman, K.M.; Aisyah, M.R.; Rahim, K.K. Antioxidant study of pulps and peels of dragon fruits: A comparative study. Int. Food Res. J. 2010, 17, 367–375. [Google Scholar]
  6. Poolsup, N.; Suksomboon, N.; Paw, N.J. Effect of dragon fruit on glycemic control in prediabetes and type 2 diabetes: A systematic review and meta-analysis. PLoS ONE 2017, 12, e0184577. [Google Scholar] [CrossRef]
  7. Attar, Ş.H.; Gündeşli, M.A.; Urün, I.; Kafkas, S.; Kafkas, N.E.; Ercisli, S.; Ge, C.; Mlcek, J.; Adamkova, A. Nutritional Analysis of Red-Purple and White-Fleshed Pitaya (Hylocereus) Species. Molecules 2022, 27, 808. [Google Scholar] [CrossRef] [PubMed]
  8. Bokulich, N.A.; Thorngate, J.H.; Richardson, P.M.; Mills, D.A. Microbial biogeography of wine grapes is conditioned by cultivar, vintage, and climate. Proc. Natl. Acad. Sci. USA 2014, 111, E139–E148. [Google Scholar] [CrossRef]
  9. Rochefort, A.; Briand, M.; Marais, C.; Wagner, M.-H.; Laperche, A.; Vallée, P.; Barret, M.; Sarniguet, A. Influence of Environment and Host Plant Genotype on the Structure and Diversity of the Brassica napus Seed Microbiota. Phytobiomes J. 2019, 3, 326–336. [Google Scholar] [CrossRef]
  10. Bonito, G.; Reynolds, H.; Robeson, M.S.; Nelson, J.; Hodkinson, B.P.; Tuskan, G.; Schadt, C.W.; Vilgalys, R. Plant host and soil origin influence fungal and bacterial assemblages in the roots of woody plants. Mol. Ecol. 2014, 23, 3356–3370. [Google Scholar] [CrossRef]
  11. Cregger, M.A.; Veach, A.M.; Yang, Z.K.; Crouch, M.J.; Vilgalys, R.; Tuskan, G.A.; Schadt, C.W. The Populus holobiont: Dissecting the effects of plant niches and genotype on the microbiome. Microbiome 2018, 6, 31. [Google Scholar] [CrossRef] [PubMed]
  12. Zhu, Q.L.; Yan, K.; Wang, N.Z.; Ma, S.Q.; Lu, D.S.; Su, X.H.; Yuan, Z.S.; Dong, Y.F.; Wang, Y.P.; Ding, C.J. The structure and assembly of rhizobacterial communities are influenced by poplar genotype. Front. Microbiol. 2022, 13, 1052567. [Google Scholar] [CrossRef] [PubMed]
  13. Liu, F.; Hewezi, T.; Lebeis, S.L.; Pantalone, V.; Grewal, P.S.; Staton, M.E. Soil indigenous microbiome and plant genotypes cooperatively modify soybean rhizosphere microbiome assembly. BMC Microbiol. 2019, 19, 201. [Google Scholar] [CrossRef] [PubMed]
  14. Qu, Z.; Li, Y.-H.; Xu, W.-H.; Chen, W.-J.; Hu, Y.-L.; Wang, Z.-G. Different genotypes regulate the microbial community structure in the soybean rhizosphere. J. Integr. Agric. 2023, 22, 585–597. [Google Scholar] [CrossRef]
  15. Malacrinò, A.; Mosca, S.; Nicosia, M.G.L.D.; Agosteo, G.E.; Schena, L. Plant Genotype Shapes the Bacterial Microbiome of Fruits, Leaves, and Soil in Olive Plants. Plants 2022, 11, 613. [Google Scholar] [CrossRef] [PubMed]
  16. Chen, S.; Qin, R.; Yang, D.; Liu, W.; Yang, S. A Comparison of Rhizospheric and Endophytic Bacteria in Early and Late-Maturing Pumpkin Varieties. Microorganisms 2022, 10, 1667. [Google Scholar] [CrossRef] [PubMed]
  17. Sun, Y.; Huang, Z.; Chen, S.; Yang, D.; Lin, X.; Liu, W.; Yang, S. Higher-Quality Pumpkin Cultivars Need to Recruit More Abundant Soil Microbes in Rhizospheres. Microorganisms 2022, 10, 2219. [Google Scholar] [CrossRef] [PubMed]
  18. Hemmerle, L.; Maier, B.A.; Bortfeld-Miller, M.; Ryback, B.; Gäbelein, C.G.; Ackermann, M.; Vorholt, J.A. Dynamic character displacement among a pair of bacterial phyllosphere commensals in situ. Nat. Commun. 2022, 13, 2836. [Google Scholar] [CrossRef] [PubMed]
  19. Qi, M.; Berry, J.C.; Veley, K.M.; O’connor, L.; Finkel, O.M.; Salas-González, I.; Kuhs, M.; Jupe, J.; Holcomb, E.; del Rio, T.G.; et al. Identification of beneficial and detrimental bacteria impacting sorghum responses to drought using multi-scale and multi-system microbiome comparisons. ISME J. 2022, 16, 1957–1969. [Google Scholar] [CrossRef]
  20. Ren, Y.; Xun, W.; Yan, H.; Ma, A.; Xiong, W.; Shen, Q.; Zhang, R. Functional compensation dominates the assembly of plant rhizospheric bacterial community. Soil Biol. Biochem. 2020, 150, 107968. [Google Scholar] [CrossRef]
  21. Igwe, A.N.; Vannette, R.L. Bacterial communities differ between plant species and soil type, and differentially influence seedling establishment on serpentine soils. Plant Soil 2019, 441, 423–437. [Google Scholar] [CrossRef]
  22. Sangiorgio, D.; Cellini, A.; Donati, I.; Ferrari, E.; Tanunchai, B.; Wahdan, S.F.M.; Sadubsarn, D.; Farneti, B.; Checcucci, A.; Buscot, F.; et al. Taxonomical and functional composition of strawberry microbiome is genotype-dependent. J. Adv. Res. 2022, 42, 189–204. [Google Scholar] [CrossRef] [PubMed]
  23. Dong, Z.; Guo, Y.; Yu, C.; Zhixian, Z.; Rongli, M.; Deng, W.; Li, Y.; Hu, X. The dynamics in rhizosphere microbial communities under bacterial wilt resistance by mulberry genotypes. Arch. Microbiol. 2021, 203, 1107–1121. [Google Scholar] [CrossRef] [PubMed]
  24. Chen, S.; Sun, Y.; Wei, Y.; Li, H.; Yang, S. Different rhizosphere soil microbes are recruited by tomatoes with different fruit color phenotypes. BMC Microbiol. 2022, 22, 210. [Google Scholar] [CrossRef] [PubMed]
  25. Xiao, J.; Chen, S.-Y.; Sun, Y.; Yang, S.-D.; He, Y. Differences of rhizospheric and endophytic bacteria are recruited by different watermelon phenotypes relating to rind colors formation. Sci. Rep. 2022, 12, 6360. [Google Scholar] [CrossRef]
  26. Santhanam, R.; Luu, V.T.; Weinhold, A.; Goldberg, J.; Oh, Y.; Baldwin, I.T. Native root-associated bacteria rescue a plant from a sudden-wilt disease that emerged during continuous cropping. Proc. Natl. Acad. Sci. USA 2015, 112, E5013–E5020. [Google Scholar] [CrossRef] [PubMed]
  27. Zhou, C.; Guo, J.; Zhu, L.; Xiao, X.; Xie, Y.; Zhu, J.; Ma, Z.; Wang, J. Paenibacillus polymyxa BFKC01 enhances plant iron absorption via improved root systems and activated iron acquisition mechanisms. Plant Physiol. Biochem. 2016, 105, 162–173. [Google Scholar] [CrossRef] [PubMed]
  28. Lau, J.A.; Lennon, J.T. Evolutionary ecology of plant–microbe interactions: Soil microbial structure alters selection on plant traits. New Phytol. 2011, 192, 215–224. [Google Scholar] [CrossRef] [PubMed]
  29. Eisenhauer, N.; Powell, J.R. Plant trait effects on soil organisms and functions. Pedobiologia 2017, 65, 1–4. [Google Scholar] [CrossRef]
  30. Zheng, X.; Liu, S.; Cheng, C.; Guo, R.; Chen, Y.; Xie, L.; Mao, Y.; Lin, Y.; Zhang, Z.; Lai, Z. Cloning and expression analysis of betalain biosynthesis genes in Amaranthus tricolor. Biotechnol. Lett. 2016, 38, 723–729. [Google Scholar] [CrossRef]
  31. Uniyal, S.; Bhandari, M.; Singh, P.; Singh, R.K.; Tiwari, S.P. Cytokinin biosynthesis in cyanobacteria: Insights for crop improvement. Front. Genet. 2022, 13, 933226. [Google Scholar] [CrossRef]
  32. Stobart, A.K.; Kinsman, L.T. The hormonal control of betacyanin synthesis in Amaranthus caudatus. Phytochemistry 1977, 16, 1139–1142. [Google Scholar] [CrossRef]
  33. Shi, T.-Q.; Peng, H.; Zeng, S.-Y.; Ji, R.-Y.; Shi, K.; Huang, H.; Ji, X.-J. Microbial production of plant hormones: Opportunities and challenges. Bioengineered 2017, 8, 124–128. [Google Scholar] [CrossRef]
  34. Yadav, A.N.; Kour, D.; Kaur, T.; Devi, R.; Yadav, A. Endophytic fungal communities and their biotechnological implications for agro-environmental sustainability. Folia Microbiol. 2022, 67, 203–232. [Google Scholar] [CrossRef] [PubMed]
  35. Zhu, C.; Jin, H.; Guo, Z.; Li, G.; Xia, K.; Xu, Z.; Ng, D.; Gan, L. Antagonistic effect of indole-3-acetic acid on kinetin-stimulated amaranthin accumulation in the cotyledons of Amaranthus mangostanus seedlings. J. Hortic. Sci. Biotechnol. 2016, 91, 196–202. [Google Scholar] [CrossRef]
  36. Dos Santos, A.Z.; Innocentini, M.D.d.M.; Lourenço, M.V. Optimization of jasmonates bioproduction. BMC Proc. 2014, 8, P208. [Google Scholar] [CrossRef]
  37. Cao, S.; Liu, T.; Jiang, Y.; He, S.; Harrison, D.K.; Joyce, D.C. The effects of host defence elicitors on betacyanin accumulation in Amaranthus mangostanus seedlings. Food Chem. 2012, 134, 1715–1718. [Google Scholar] [CrossRef]
  38. Matoba, Y.; Kumagai, T.; Yamamoto, A.; Yoshitsu, H.; Sugiyama, M. Crystallographic Evidence That the Dinuclear Copper Center of Tyrosinase Is Flexible during Catalysis. J. Biol. Chem. 2006, 281, 8981–8990. [Google Scholar] [CrossRef] [PubMed]
  39. Sendovski, M.; Kanteev, M.; Ben-Yosef, V.S.; Adir, N.; Fishman, A. First Structures of an Active Bacterial Tyrosinase Reveal Copper Plasticity. J. Mol. Biol. 2011, 405, 227–237. [Google Scholar] [CrossRef]
  40. Ismaya, W.T.; Rozeboom, H.J.; Weijn, A.; Mes, J.J.; Fusetti, F.; Wichers, H.J.; Dijkstra, B.W. Crystal Structure of Agaricus bisporus Mushroom Tyrosinase: Identity of the Tetramer Subunits and Interaction with Tropolone. Biochemistry 2011, 50, 5477–5486. [Google Scholar] [CrossRef]
  41. Nabi, B.G.; Mukhtar, K.; Ahmed, W.; Manzoor, M.F.; Ranjha, M.M.A.N.; Kieliszek, M.; Bhat, Z.F.; Aadil, R.M. Natural pigments: Anthocyanins, carotenoids, chlorophylls, and betalains as colorants in food products. Food Biosci. 2023, 52, 102403. [Google Scholar] [CrossRef]
  42. Grewal, P.S.; Modavi, C.; Russ, Z.N.; Harris, N.C.; Dueber, J.E. Bioproduction of a betalain color palette in Saccharomyces cerevisiae. Metab. Eng. 2018, 45, 180–188. [Google Scholar] [CrossRef] [PubMed]
  43. Wang, H.; Li, Y.; Zhang, K.; Ma, Y.; Li, P. Feasibility and transcriptomic analysis of betalain production by biomembrane surface fermentation of Penicillium novae-zelandiae. AMB Express 2018, 8, 4. [Google Scholar] [CrossRef] [PubMed]
  44. Edwards, J.; Johnson, C.; Santos-Medellín, C.; Lurie, E.; Podishetty, N.K.; Bhatnagar, S.; Eisen, J.A.; Sundaresan, V. Structure, variation, and assembly of the root-associated microbiomes of rice. Proc. Natl. Acad. Sci. USA 2015, 112, E911–E920. [Google Scholar] [CrossRef] [PubMed]
  45. El Zahar Haichar, F.; Marol, C.; Berge, O.; Rangel-Castro, J.I.; Prosser, J.I.; Balesdent, J.M.; Heulin, T.; Achouak, W. Plant host habitat and root exudates shape soil bacterial community structure. ISME J. 2008, 2, 1221–1230. [Google Scholar] [CrossRef] [PubMed]
  46. Baudoin, E.; Nazaret, S.; Mougel, C.; Ranjard, L.; Moënne-Loccoz, Y. Impact of inoculation with the phytostimulatory PGPR Azospirillum lipoferum CRT1 on the genetic structure of the rhizobacterial community of field-grown maize. Soil Biol. Biochem. 2009, 41, 409–413. [Google Scholar] [CrossRef]
  47. Semchenko, M.; Xue, P.; Leigh, T. Functional diversity and identity of plant genotypes regulate rhizodeposition and soil microbial activity. New Phytol. 2021, 232, 776–787. [Google Scholar] [CrossRef] [PubMed]
  48. Ndour, P.M.S.; Barry, C.M.; Tine, D.; Cantó, C.D.l.F.; Gueye, M.; Barakat, M.; Ortet, P.; Achouak, W.; Ndoye, I.; Sine, B.; et al. Pearl millet genotype impacts microbial diversity and enzymatic activities in relation to root-adhering soil aggregation. Plant Soil 2021, 464, 109–129. [Google Scholar] [CrossRef]
  49. Wagner, M.R.; Lundberg, D.S.; del Rio, T.G.; Tringe, S.G.; Dangl, J.L.; Mitchell-Olds, T. Host genotype and age shape the leaf and root microbiomes of a wild perennial plant. Nat. Commun. 2016, 7, 12151. [Google Scholar] [CrossRef]
  50. Eisenhauer, N.; Lanoue, A.; Strecker, T.; Scheu, S.; Steinauer, K.; Thakur, M.P.; Mommer, L. Root biomass and exudates link plant diversity with soil bacterial and fungal biomass. Sci. Rep. 2017, 7, srep44641. [Google Scholar] [CrossRef]
  51. Sokol, N.W.; Kuebbing, S.E.; Karlsen-Ayala, E.; Bradford, M.A. Evidence for the primacy of living root inputs, not root or shoot litter, in forming soil organic carbon. New Phytol. 2019, 221, 233–246. [Google Scholar] [CrossRef] [PubMed]
  52. Gmoser, R.; Ferreira, J.A.; Lennartsson, P.R.; Taherzadeh, M.J. Filamentous ascomycetes fungi as a source of natural pigments. Fungal Biol. Biotechnol. 2017, 4, 4. [Google Scholar] [CrossRef]
  53. Méndez, A.; Pérez, C.; Montañéz, J.C.; Martínez, G.; Aguilar, C.N. Red pigment production by Penicillium purpurogenum GH2 is influenced by pH and temperature. J. Zhejiang Univ. B 2011, 12, 961–968. [Google Scholar] [CrossRef]
  54. Poorniammal, R.; Prabhu, S.; Dufossé, L.; Kannan, J. Safety Evaluation of Fungal Pigments for Food Applications. J. Fungi 2021, 7, 692. [Google Scholar] [CrossRef]
  55. Meruvu, H.; dos Santos, J.C. Colors of life: A review on fungal pigments. Crit. Rev. Biotechnol. 2021, 41, 1153–1177. [Google Scholar] [CrossRef] [PubMed]
  56. De Oliveira, L.A.; Segundo, W.O.P.F.; de Souza, É.S.; Peres, E.G.; Koolen, H.H.F.; de Souza, J.V.B. Ascomycota as a source of natural colorants. Braz. J. Microbiol. 2022, 53, 1199–1220. [Google Scholar] [CrossRef]
  57. Rúa, M.A.; Antoninka, A.; Antunes, P.M.; Chaudhary, V.B.; Gehring, C.; Lamit, L.J.; Piculell, B.J.; Bever, J.D.; Zabinski, C.; Meadow, J.F.; et al. Home-field advantage? evidence of local adaptation among plants, soil, and arbuscular mycorrhizal fungi through meta-analysis. BMC Evol. Biol. 2016, 16, 122. [Google Scholar] [CrossRef] [PubMed]
  58. Fitzpatrick, C.R.; Copeland, J.; Wang, P.W.; Guttman, D.S.; Kotanen, P.M.; Johnson, M.T.J. Assembly and ecological function of the root microbiome across angiosperm plant species. Proc. Natl. Acad. Sci. USA 2018, 115, E1157–E1165. [Google Scholar] [CrossRef]
  59. Mapari, S.A.S.; Hansen, M.E.; Meyer, A.S.; Thrane, U. Computerized Screening for Novel Producers of Monascus-like Food Pigments in Penicillium Species. J. Agric. Food Chem. 2008, 56, 9981–9989. [Google Scholar] [CrossRef]
  60. Mussagy, C.U.; Winterburn, J.; Santos-Ebinuma, V.C.; Pereira, J.F.B. Production and extraction of carotenoids produced by microorganisms. Appl. Microbiol. Biotechnol. 2019, 103, 1095–1114. [Google Scholar] [CrossRef]
  61. Simonin, M.; Dasilva, C.; Terzi, V.; Ngonkeu, E.L.M.; Diouf, D.; Kane, A.; Béna, G.; Moulin, L. Influence of plant genotype and soil on the wheat rhizosphere microbiome: Evidences for a core microbiome across eight African and European soils. FEMS Microbiol. Ecol. 2020, 96, fiaa67. [Google Scholar] [CrossRef] [PubMed]
Plants 13 01346 g001
Figure 1. The appearance and morphological characteristics of dragon fruit varieties with white and red flesh. (A): Nanning white-flesh (H. undatus, RW); (B): YuanzhiHong red-flesh (H. polyrhizus, RR).
Figure 1. The appearance and morphological characteristics of dragon fruit varieties with white and red flesh. (A): Nanning white-flesh (H. undatus, RW); (B): YuanzhiHong red-flesh (H. polyrhizus, RR).
Plants 13 01346 g001
Plants 13 01346 g002
Figure 2. Comparison of the soil bacterial and fungal compositions among RW, RR, and CK. PCoA of soil bacterial (A) and fungal (C) communities at the OTU level. PLS-DA score plot of the soil bacterial (B) and fungal (D) communities among RW, RR, and CK.
Figure 2. Comparison of the soil bacterial and fungal compositions among RW, RR, and CK. PCoA of soil bacterial (A) and fungal (C) communities at the OTU level. PLS-DA score plot of the soil bacterial (B) and fungal (D) communities among RW, RR, and CK.
Plants 13 01346 g002
Plants 13 01346 g003
Figure 3. Distributions of dominant soil bacteria in the rhizospheres at the phylum (A) and genus (B) levels among RW, RR, and CK.
Figure 3. Distributions of dominant soil bacteria in the rhizospheres at the phylum (A) and genus (B) levels among RW, RR, and CK.
Plants 13 01346 g003
Plants 13 01346 g004
Figure 4. Distributions of dominant soil fungi in the rhizospheres at the phylum (A) and genus (B) levels among RW, RR, and CK.
Figure 4. Distributions of dominant soil fungi in the rhizospheres at the phylum (A) and genus (B) levels among RW, RR, and CK.
Plants 13 01346 g004
Plants 13 01346 g005
Figure 5. LEfSe analysis of soil bacteria among RW, RR, and CK. Different prefixes indicate different levels (p: phylum; c: class, o: order; f: family; g: genus).
Figure 5. LEfSe analysis of soil bacteria among RW, RR, and CK. Different prefixes indicate different levels (p: phylum; c: class, o: order; f: family; g: genus).
Plants 13 01346 g005
Plants 13 01346 g006
Figure 6. LEfSe analysis of soil fungi among RW, RR, and CK. Different prefixes indicate different levels (p: phylum; c: class, o: order; f: family; g: genus).
Figure 6. LEfSe analysis of soil fungi among RW, RR, and CK. Different prefixes indicate different levels (p: phylum; c: class, o: order; f: family; g: genus).
Plants 13 01346 g006
Plants 13 01346 g007
Figure 7. Relative abundance statistics and test for significant differences in soil bacterial expression in the top 10 MetaCycpathway functions among RW, RR, and CK. (A): CK vs. RW; (B): CK vs. RR; (C): RW vs. RR.
Figure 7. Relative abundance statistics and test for significant differences in soil bacterial expression in the top 10 MetaCycpathway functions among RW, RR, and CK. (A): CK vs. RW; (B): CK vs. RR; (C): RW vs. RR.
Plants 13 01346 g007
Plants 13 01346 g008
Figure 8. Functional predictions of soil fungal communities among RW, RR, and CK.
Figure 8. Functional predictions of soil fungal communities among RW, RR, and CK.
Plants 13 01346 g008
Table 1. Diversity of soil microbes in the rhizospheres of H. undatus and H. polyrhizus.
Table 1. Diversity of soil microbes in the rhizospheres of H. undatus and H. polyrhizus.
TreatmentShannonInvsimpsonAceChaoCoverage
Soil bacteriaRW6.39 ± 0.04 a183.7 ± 25.89 a3229 ± 23.96 a3075 ± 29.39 a0.98
RR6.40 ± 0.03 a187.4 ± 19.37 a3120 ± 16.27 a3189 ± 27.66 a0.98
CK6.29 ± 0.30 a196.0 ± 60.66 a3046 ± 200.7 a3002 ± 169.6 a0.98
Soil fungiRW3.53 ± 0.43 a10.65 ± 2.391 a859.3 ± 8.13 a854.8 ± 26.68 b0.99
RR3.76 ± 0.31 a8.857 ± 3.796 a807.8 ± 17.02 a825.4 ± 13.58 b0.99
CK4.41 ± 0.18 a26.06 ± 8.993 a912.6 ± 50.67 a925.3 ± 37.60 a0.99
Note: Data in the table are presented as the means ± SDs; values followed by different lowercase letters indicate significant differences at p < 0.05 among RW, RR, and CK (RW: H. undatus, RR: H. polyrhizus, CK: background; the same below).
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content.

Share and Cite

MDPI and ACS Style

Zhou, X.; Chen, S.; Qiu, L.; Liao, L.; Lu, G.; Yang, S. How Rhizosphere Microbial Assemblage Is Influenced by Dragon Fruits with White and Red Flesh. Plants 2024, 13, 1346. https://doi.org/10.3390/plants13101346

AMA Style

Zhou X, Chen S, Qiu L, Liao L, Lu G, Yang S. How Rhizosphere Microbial Assemblage Is Influenced by Dragon Fruits with White and Red Flesh. Plants. 2024; 13(10):1346. https://doi.org/10.3390/plants13101346

Chicago/Turabian Style

Zhou, Xinyan, Siyu Chen, Lulu Qiu, Liyuan Liao, Guifeng Lu, and Shangdong Yang. 2024. "How Rhizosphere Microbial Assemblage Is Influenced by Dragon Fruits with White and Red Flesh" Plants 13, no. 10: 1346. https://doi.org/10.3390/plants13101346

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