Hindawi
Advances in Agriculture
Volume 2024, Article ID 9977517, 8 pages
https://doi.org/10.1155/2024/9977517
Research Article
Arbuscular Mycorrhizal Fungi Associated with
Myrciaria dubia in the Amazonia Region, Peru
Alexandra Jherina Pineda-Lázaro ,1 Adela Vallejos-Tapullima ,1
Angel David Hernández-Amasifuen ,1 Santos Carballar-Hernández ,2
Sixto Imán-Correa ,3,4 Fernando Marcelo Carvajal-Vallejos ,5 Orlando Ríos-Ramírez ,1
and Mike Anderson Corazon-Guivin 1
1Laboratorio de Biología y Genética Molecular, Universidad Nacional de San Martín, Tarapoto, Jr. Amorarca 315, Morales, 22201,
San Martin, Peru
2Universidad de la Ciénega del Estado de Michoacán de Ocampo, Avenida Universidad, 3000, Col. Lomas de la Universidad, 59103,
Sahuayo, Michoacán, Mexico
3Dirección de Recursos Genéticos y Biotecnología, Instituto Nacional de Innovación Agraria, Av. la Molina N° 1981,
Lima 15024, Peru
4Universidad Nacional de la Amazonía Peruana, Av. Grau 1072, Iquitos 16001, Loreto, Peru
5Unidad de Limnología y Recursos Acuáticos (ULRA), Departamento de Biología, Facultad de Ciencias y Tecnología (FCyT),
Universidad Mayor de San Simón (UMSS), Calle Sucre Frente al Parque La Torre S/N., Cochabamba, Bolivia
Correspondence should be addressed to Mike Anderson Corazon-Guivin; macorazong@unsm.edu.pe
Received 14 August 2023; Revised 30 December 2023; Accepted 16 January 2024; Published 30 January 2024
Academic Editor: Amelia Salimonti
Copyright © 2024 Alexandra Jherina Pineda-Lázaro et al. This is an open access article distributed under the Creative Commons
Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is
properly cited.
Myrciaria dubia (Kunth) McVaugh (camu-camu) is a shrub native to the Amazon region that produces fruits with a high content
of vitamin C and various bioactive compounds, making it a functional food with antioxidant, anti-inflammatory, and antimicrobial
properties. However, it is unknown which microorganisms are associated with its root system and can influence its growth and
productivity. Arbuscular mycorrhizal fungi (AMF) are associated with most plants and are essential for their establishment,
survival, and productivity since they facilitate their nutrition, increase water absorption, and improve soil structure. Although
the AMF association is already known in some species ofMyrciaria, no report is available on its association inM. dubia. This study
presents, for the first time, the symbiotic association between AMF and M. dubia from the INIA San Roque experimental station
located in the Amazon region, Peru. For the morphological and molecular analyses of the AMF, samples of rhizospheric soil and
roots from two native accessions of the National Germplasm Bank ofM. dubia were collected. Eighteen AMF morphospecies were
identified in rhizospheric soil, belonging to nine genera Acaulospora, Ambispora, Entrophospora, Diversispora, Gigaspora, Glomus,
Paraglomus, Funneliformis, and Sclerocystis, being the first one the most frequent. The roots ofM. dubia showed high colonization
by AMF (mean= 91%), and characteristic structures of arbuscular mycorrhizae, such as vesicles, hyphae, and arbuscules, could be
observed. Likewise, the molecular analysis detected the presence of genetic material (rDNA) corresponding to AMF in the roots of
both accessions. Our results evidenced the symbiotic association between AMF and M. dubia, which encourages further investi-
gation of the functional potential of these microorganisms in this economically crucial agricultural plant in Peru.
1. Introduction
Myrciaria dubia (Kunt) McVaugh, popularly known as camu found naturally in flooded environments near streams or rivers
camu, is native to the Amazon region of Peru, Brazil, Venezuela, in the Amazon region [3–5]. However, it is cultivated in agricul-
and Colombia [1], and its most prominent natural population is tural areas (nonflooded lands) in association with other crops
located in the eastern Peruvian Amazon [2]. It is a shrub species [6], demonstrating good adaptive capacity [7].
2 Advances in Agriculture
The pulp of the M. dubia fruit has a tremendous nutri- polyethylene bags in a cooler at 4°C and then transported to
tional potential that lies in the high concentration of ascorbic the biology and molecular genetics laboratories at the National
acid (vitamin C), higher than other fruits such as acerola, University of SanMartín (Tarapoto, Peru). In the laboratory, the
lemon, and orange [8]. This fruit is consumed worldwide as roots and soil were separated. The roots were pooled in a sample
a beverage, frozen pulp, or extract [1, 9]. Likewise, it presents composed of each accession, washed, dried with paper, cut into
antioxidant [10], anti-inflammatory [1], and photoprotective 1–2 cm pieces, and homogenized in water. Two 200mg aliquots
[11] properties. Consequently, almost all research on this were frozen at −80°C for molecular analysis. The remaining
species has focused on its nutraceutical, pharmaceutical, roots were kept in ethanol at 70° to determine mycorrhizal
and cosmetological properties, with few studies on the diver- colonization. Soil samples were also mixed for each accession,
sity of microbial communities present in the rhizosphere of dried at room temperature for 48hr, and sieved through a 5-mm
this plant. mesh to remove root debris and stones. Finally, they were stored
Among the microbial communities, the arbuscular mycor- in airtight bags and kept at 4°C until use.
rhizal fungi (AMF) stand out [12], which are associated with
approximately 80% of plant species in almost all terrestrial eco- 2.2. Morphological Analyses. The isolation and specimen
systems [13, 14]. This association is de ned as an obligatory preparation were performed according to Corazon-Guivinfi
mutualistic symbiotic relationship that inhabits the root cells et al. [34]. For the morphological identification of AMF,
of the host plant [15], improving the uptake of P, N, S, K, and the classification proposed by Oehl et al. [39] was followed,
various microelements (Fe, Cu, Zn, and many other minerals) and the taxonomic organization of orders, families, and gen-
[16]. Likewise, it provides resistance against pathogens and unfa- era suggested by Blaszkowski et al. [40] and Wijayawardene
vorable environmental conditions and improves soil quality [17]. et al. [41] was followed.
Root colonization by AMF is characterized by presenting 2.3. Fungal Intraradical Colonization. Approximately 5 g
fungal structures, such as mycelium, auxiliary cells, arbus- from the roots of each accession were stained, according to
cules, vesicles, and spores [18, 19], being this vast structure it Vierheilig et al. [43]. Once stained, the roots were cut into
is most important for its correct identification using the 1 cm segments, mounted on slides, and examined in a com-
morphological approach [18–22]. Currently, in the Peruvian pound microscope (20x) by intersection method [44].
Amazon, some studies have recorded a great diversity of
AMF [23 27]. New species were identified in different crops 2.4. Molecular Analysis. DNA was extracted from 100mg fine–
[23, 28 38] using morphological and molecular tools roots (a mix of the three plants for each accession) using the–
[39 41], and molecular analyses of the SSU-ITS-LSU region cetyltrimethylammonium bromide (CTAB) protocol. Subse-–
of rDNA [42]. quently, a two-step PCR (using gDNA) was conducted to
In this context, to know the symbiotic association between amplify the ribosomal fragment of AMF consisting of partial
AMF and M. dubia, we evaluated: (i) the presence of intrara- SSU, ITS1, 5.8S, ITS2, and partial LSU rDNA using the primers
dical fungal structures typical of AMF symbiosis: vesicles, SSUmAf/LSUmAr and SSUmCf/LSUmBr, consecutively [42].
hyphae, and arbuscules; (ii) the presence of AMF rDNA inside The PCR was carried out according to Corazon-Guivin et al.
the roots ofM. dubia; and (iii) diversity of AMF species present [23, 28–34]. PCR products from the second round of amplifica-
in M. dubia rhizospheric soil in the Amazonas region, Peru. tions (∼1500bp) were separated by electrophoresis on 1.2%
agarose gel, stained with Diamond™ Nucleic Acid Dye
2. Materials and Methods (Promega), and revealed by UV illumination.
2.1. Soil Collection and Conservation. The sampling was car- 2.5. Comparative Analysis. Sørensen index was used to assess
ried out in two elite accessions (which exhibited the best agro- the similarity of AMF species among accessions. The Venn
nomic qualities, such as percent pulp, fruit weight, ascorbic acid diagram was constructed using the calculate and draw cus-
tom Venn diagrams tool available online (http://bioinforma
content, and yield. These accessions gave rise to the first variety
tics.psb.ugent.be/webtools/Venn/).
of M. dubia “INIA 395-Vitahuayo,” https://www.gob.pe/
institucion/inia/noticias/349846) of the National Germplasm 3. Results and Discussion
bank of M. dubia of the Agrarian Experimental Station “San
Roque” Iquitos, National Institute of Agrarian Innovation According to the morphological and molecular analyses, the
(INIA) (Figure 1). This station is located at 25 km of the mutualistic symbiotic relationship between AMF and M. dubia
Iquitos–Nauta highway (03°57’17” S, 73°24’55” W, 112m of was evidenced for the first time. Likewise, we report the taxo-
elevation) and has a sandy loam texture soil, pH= 4.10, M.O nomic diversity of AMF associated with two accessions from the
= 1.63%, and P= 3.01ppm (Supplementary 1). The M. dubia National Germplasm Bank of M. dubia, Peru. Previous studies
accessions were introduced from plant material collected from showed that species of the genus Myrciaria establish symbiosis
native populations located in the Loreto region (Table 1). The withAMF. For example, a study evaluatedM. cauliflora plants in
biological samples were composed of 1.5 kg of rhizospheric soil the field and reported 40% root colonization [45]. In the same
and 10 g of root tissue, which were extracted from three random way, it was observed that M. glomerata seedlings, under con-
plants for each accession. From each plant, subsamples were trolled conditions, showed similar results [46]. In our study,
collected from three equidistant points around the main stem AMF root colonization reached a mean value of 91%. We
from 0 to 20 cm deep, which were mixed and stored in were able to observe the presence of different typical AMF
Advances in Agriculture 3
73°39´0˝W 73°30´0˝W 73°21´0˝W
South
America
N Accession: Yuto District
Accession: Samito boundary
W E National Germplasm Bank of Altitude (m.a.s.l)
Loreto Myrciaria dubia <130
region S River 130–180
Camu camu 0 2 4 8 12 Lake >180
(Myrciaria dubia) km
FIGURE 1: Spatial location of the National Germplasm Bank ofM. dubia (Kunth) McVaugh at the Agrarian Experimental Station “San Roque”
in Loreto Region, National Institute of Agrarian Innovation (INIA).
TABLE 1: Origin sites of the elite accessions from the National Germplasm Bank ofM. dubia (Kunth) McVaugh at the Agrarian Experimental
Station “San Roque” in Iquitos, National Institute of Agrarian Innovation (INIA), Peru.
Department Province District Basin Location Codnac Codentban Coordinates
3°51’18.3” S
Samito PER1000394 MD-014
73°35’4.5” W
Loreto Maynas San Juan Bautista Nanay
3°53’22.9” S
Yuto PER1000395 MD-015
73°31’5.0” W
structures, i.e. hyphae, vesicles, and intraradical arbuscules species: D. aurantia, D. eburnea, D. invermanium, and
(Figure 2). Also, we provide molecular evidence on the presence D. tortuosa, andAmbisporawith three species:A. appendicula,
of AMF in roots ofM. dubia (Figure 3). This analysis was carried A. reticulata, and an unidentified one. Furthermore, Funneli-
out using the primers SSUmAf/LSUmAr and SSUmCf/LSUmBr formis geosporus, Glomus macrocarpum, Sclerocystis sinuo-
[38], which amplify a much more informative region of rDNA sum, Entrophospora etunicata, Gigaspora margarita, and
than is typically used for root-level molecular analysis [47]. Paraglomus sp. were found (Figure 4). The presence of possi-
We found a total of 18AMF species belonging to nine genera ble unidentified new species could be related to the fact of an
and seven families in the rhizospheric soil of two M. dubia area not yet characterized and a poorly studied plant species.
accessions (Supplementary 2).Acaulospora is themost dominant Thus, our research group recently recently reported 11 new
genus, with five species: A. mellea, A. morrowiae, A. undulata, AMF species in the Peruvian Amazon such as Funneliglomus
and two unidentified species. Diversispora followed it with four sanmartinensis, Microkamienskia peruviana, Acaulospora
4°3´0˝S 3°54´0˝S 3°45´0˝S
4°3´0˝S 3°54´0˝S 3°45´0˝S
4 Advances in Agriculture
200 μm 100 μm 50 μm
ðaÞ ðbÞ ðcÞ
FIGURE 2: Arbuscular mycorrhizal colonization inM. dubia (Kunth) McVaugh: (a) extraradical hyphae of arbuscular mycorrhizal; (b) vesicles
in roots; and (c) branched arbuscles.
M 1 + 2 + – 1 + 2 + M –
1,500 pb
ðaÞ ðbÞ
FIGURE 3: Gel electrophoresis. (a) Carril 1: (M) 1 kb molecular marker (Invitrogen, USA), Carril 2−3: (1+, 2+) AMF genomic DNA, Carril 4:
(−) negative control, no DNA was added; (b) PCR reaction, Carril 1−2: (1+, 2+) 1,500 bp fragment of AMF DNA, Carril 3: (M) 1 kb
molecular marker (Invitrogen, USA), Carril 4: (−) negative control reaction, no DNA was added.
aspera,Nanoglomus plukenetiae, Rhizoglomus variabile, Para- sampling area is classified as ultisol. In this regard, Veresoglou
glomus occidentale, Acaulospora flava, Paraglomus peruvia- et al. [53] and Coutinho et al. [54] mentioned that the genus
num, Acaulospora flavopapillosa, Rhizoglomus cacao, and Acaulospora is adapted to an acid soil pH (<5.0). Likewise, the
Diversispora alba [28–38]. A study conducted in three agroe- absence of species from the Rhizoglomus genus in our study
cosystems associated with Theobroma cacao in the Peruvian could be influenced by pH, as certain limitations in the growth
Amazon rainforest reported 46 AMF species [48].Meanwhile, of some species of this genus in slightly acidic soil have been
another study carried out in the Colombian Amazon rain- reported [55].
forest reported 18 AMF species, similar to the species richness Among the 18 AMF species identified, two were found
found in our study [49]. exclusively in the rhizospheric soil of Samito, six species in
Approximately, 65% of the soils of the Amazon lowlands the rhizospheric soil of Yuto, and 12 AMF species were
in Peru are classified as ultisols, characterized by being shared between both accessions (Figure 5). The high percent-
extraordinarily acidic and having low availability of phos- age of similarity (67%) of AMF species can be attributed to
phorus [50]. The pH can exert a fundamental influence on the proximity of both accessions within the Germplasm
the composition and diversity of bacteria and fungi living in bank, exhibiting similar edaphoclimatic properties. In their
the soil, owing to its direct impact on the regulation and study, Vieira et al. [56] demonstrated a higher percentage of
mobilization of several essential nutrients [23, 51]. In this similarity of AMF species in two ecosystems that shared
context, AM symbiosis constitutes a key strategy to help similar soil properties. Furthermore, the presence of certain
plants efficiently take up phosphorus from the soil [52]. In AMF species exclusively in the rhizospheric soil of one acces-
this type of ecosystem, it has been reported that the genus sion and not the other could indicate that the genotype of
Acaulospora is abundant [48], similar to our study, where the each accession might have an influence. In this regard,
Advances in Agriculture 5
(a) (b) (c) (d)
50 μm
50 μm
50 μm 50 μm
(e) (f) (g) (h) (i)
50 μm 50 μm 50 μm50 μm 50 μm
(j) (k) (l) (m)
50 μm 50 μm 50 μm 50 μm
(n) (o) (p) (q)
50 μm 50 μm
50 μm 50 μm
FIGURE 4: AMF species in M. dubia (Kunth) McVaugh: (a) Entrophospora etunicata; (b) Acaulospora morrowiae (c) Acaulospora sp1.∗;
(d) Acaulospora sp2.∗; (e) Paraglomus sp.; (f ) Ambispora appendicula; (g) Diversispora eburnea; (h) Acaulospora mellea, (i) Diversispora
tortuosa; (j) Diversispora aurantia; (k) Diversispora invermanium; (l) Funneliformis geosporum; (m) Sclerocystis sinuosum; (n) Gigaspora
margarit; (o) Glomus macrocarpum; (p) Ambispora sp.∗; (q) Ambispora reticulata. (∗) still unidentified.
Carrascosa et al. [57] also demonstrated that purslane geno- root system of this plant. Likewise, molecular techniques
types from different geographical areas can significantly allowed the confirmation of the presence of AMF inM. dubia
influence the composition of microbial communities in their roots, at the time of sampling. On the other hand, in soil
rhizospheres. samples, it was possible to identify a high diversity of AMF
associated with the rhizosphere ofM. dubia, the Acaulospora
4. Conclusions genus being the richest in morphospecies. Our results indi-
cate that AMF may play a very important role in the estab-
Our study reports and describes, for the first time, the inter- lishment, nutrition, and productivity of M. dubia cultures,
action between AMF and M. dubia through the observation which is why it is important to carry out research to elucidate
of structures such as hyphae, vesicles, and arbuscules in the the functional role of these fungi in the flow of nutrients
6 Advances in Agriculture
Samito Yuto
Acaulospora undulata
Acaulospora sp. 2
Acaulospora sp. 1 Diversispora tortuosa2 10 6 Sclerocystis sinuosum
Ambispora appendicula Entrophospora etunicata
Gigaspora margarita
Ambispora reticulata Acaulospora mellea
Ambispora sp. Acaulospora morrowiae
Funneliformis geosporus Diversispora aurantia
Glomus macrocarpum Diversispora eburnea
Paraglomus sp. Diversispora invermanium
FIGURE 5: Venn diagram showing the AMF species richness (exclusive and shared) in the rhizospheric soil of the Samito and Yuto accessions
of M. dubia (Kunth) McVaugh.
between the soil and plant. This will help to propose better References
strategies for the use, management, and formulation of
inoculants that promote sustainable production of M. dubia [1] P. C. Langley, J. V. Pergolizzi Jr., R. Taylor Jr., and
crops in Peru. C. Ridgway, “Antioxidant and associated capacities of camu
camu (Myrciaria dubia): a systematic review,” Journal of
Alternative and Complementary Medicine, vol. 21, no. 1,
Data Availability pp. 8–14, 2015.
[2] E. Arellano-Acuña, I. Rojas-Zavaleta, and L. Paucar-Menacho,
The data used to support the findings of this study are avail-
“Camu-camu (Myrciaria dubia): fruta tropical de excelentes
able from the corresponding author upon request. propiedades funcionales que ayudan a mejorar la calidad de
vida,” Scientia Agropecuaria, vol. 7, no. 4, pp. 433–443, 2016.
Conflicts of Interest [3] L. Azevedo, P. F. de Araujo Ribeiro, J. A. de Carvalho Oliveira
et al., “Camu-camu (Myrciaria dubia) from commercial
The author and co-authors declare that there are no conflicts cultivation has higher levels of bioactive compounds than
of interest regarding the publication of this paper. native cultivation (Amazon forest) and presents antimutagenic
effects in vivo,” Journal of the Science of Food and Agriculture,
Acknowledgments vol. 99, no. 2, pp. 624–631, 2018.
[4] M. Fidelis, J. S. Santos, G. B. Escher et al., “In vitro antioxidant
The authors thank all the members of the Laboratorio de and antihypertensive compounds from camu-camu (Myr-
Biología y Genética Molecular for collaborating in the publi- ciaria dubia McVaugh, Myrtaceae) seed coat: a multivariate
cation of this article. The study was supported by the Insti- structure-activity study,” Food and Chemical Toxicology,
tuto de Investigación y Desarrollo (IIyD) of the UNSM-T vol. 120, no. 1, pp. 479–490, 2018.
(Resolución No. 611-2022-UNSM/CU-R). [5] A. Fujita, V. Souza, L. Daza, C. Fávaro-Trindade, D. Granato,
and M. Genovese, “Effects of spray-drying parameters on
in vitro functional properties of camucamu (Myrciaria dubia
Supplementary Materials Mc. Vaugh): a typical Amazonian fruit,” Journal of Food
Science, vol. 82, no. 5, pp. 1083–1091, 2017.
Supplementary 1. Table 1: physical–chemical soil properties [6] M. Pinedo Panduro, C. Linares Bensimón, H. Mendoza
of the National Germplasm Bank of M. dubia (Kunth) Zuñiga, and R. Anguiz, Plan de Mejoramiento Genético de
McVaugh at the Agrarian Experimental Station “San Roque” Camu Camu, Instituto de Investigaciones de la Amazonia
in Loreto Region, National Institute of Agrarian Innovation Peruana, Iquitos, Perú, 2004.
(INIA). [7] C. Abanto-Rodriguez, M. Pinedo-Panduro, E. Alves-Chagas
et al., “Relation between the mineral nutrients and the vitamin
Supplementary 2. Table 2: abundance, richness of species, C content in camu-camu plants (Myrciria dubia) cultivated on
and colonization of arbuscular mycorrhizal fungi in the rhi- high soils and flood soils of Ucayali,” Scientia Agropecuaria,
zospheric soil of two elite accessions from the National vol. 7, no. 3, pp. 297–304, 2016.
Germplasm Bank of M. dubia (Kunth) McVaugh of the [8] L. K. O. Yuyama, J. P. L. Aguiar, K. Yuyama et al., “Teores de
Agrarian Experimental Station “San Roque” Iquitos, of the elementos minerais em algumas populações de camu-camu,”
National Institute of Agrarian Innovation (INIA). Acta Amazônica, vol. 33, no. 1, pp. 549–554, 2003.
Advances in Agriculture 7
[9] M. Hermann, “The impact of the european novel food in Peru,” Journal of Soil Science and Plant Nutrition, vol. 22,
regulation on trade and food innovation based on traditional pp. 4784–4797, 2022.
plant foods from developing countries,” Food Policy, vol. 34, [24] S. Rengifo-Del Aguila, A. De la Sota-Ricaldi, M. Corazon-
no. 6, pp. 499–507, 2009. Guivin, and Á. López-García, “Phylogenetic diversity of
[10] D. Fracassetti, C. Costa, L. Moulay, and F. A. Tomás- arbuscular mycorrhizal fungal communities increases with
Barberán, “Ellagic acid derivatives, ellagitannins, proantho- crop age in Coffea arábica plantations,” Journal of Soil
cyanidins and other phenolics, vitamin C and antioxidant Science and Plant Nutrition, vol. 22, no. 1, pp. 3291–3303,
capacity of two powder products from camu-camu fruit 2022.
(Myrciaria dubia),” Food Chemistry, vol. 139, no. 1–4, [25] N. Diagne, M. Ngom, P. Djighaly, D. Fall, V. Hocher, and
pp. 578–588, 2013. S. Svistoonoff, “Roles of arbuscular mycorrhizal fungi on plant
[11] V. Doroteo, C. Terry, C. Díaz, A. Vaisberg, and R. Rojas, growth and performance: importance in biotic and abiotic
“Compuestos fenólicos y actividades antioxidante, antielas- stressed regulation,” Diversity, vol. 12, no. 10, Article ID 370,
tasa, anticolagenasa y fotoprotectora in vitro de Myrciaria 2020.
dubia (camu camu) y Caesalpinia spinosa (tara),” Revista de la [26] A. M. de la Sota Ricaldi, S. Rengifo Del Águila, R. Blas
Sociedad Química del Perú, vol. 78, no. 4, pp. 254–263, 2012. Sevillano, Á. López-García, and M. A. Corazon-Guivin, “Beta
[12] M. C. Brundrett and L. Tedersoo, “Evolutionary history of diversity of arbuscular mycorrhizal communities increases in
mycorrhizal symbioses and global host plant diversity,” New time after crop establishment of Peruvian sacha inchi
Phytologist, vol. 220, no. 4, pp. 1108–1115, 2018. (Plukenetia volubilis),” Journal of Fungi, vol. 9, no. 2,
[13] J. Taylor, T. Helgason, and M. Öpik, “Molecular community Article ID 194, 2023.
ecology of arbuscular mycorrhizal fungi,” in The Fungal [27] B. Luis-Alaya, M. Toro, R. Calsina et al., “Evaluation of the
Community: Its Organization and Role in the Ecosystem, presence of arbuscular mycorrhizae and cadmium content in
J. Dighton and J. F. White, Eds., pp. 1–26, CRC Press Taylor& the plants and soils of cocoa plantations in San Martin, Peru,”
Francis, Fourth edition, 2017. Diversity, vol. 15, no. 2, Article ID 246, 2023.
[14] F. F. Martín, J. J. Molina, E. N. Nicolás et al., “Application of [28] M. A. Corazon-Guivin, A. C. Mendoza, J. C. Guerrero-Abad
arbuscular mycorrhizae Glomus iranicum var. tenuihypharum et al., “Funneliglomus, gen. nov., and Funneliglomus sanmar-
var. nova in intensive agriculture: a study case,” Journal of tinensis, a new arbuscular mycorrhizal fungus from the
Agricultural Science and Technology, vol. 7, pp. 221–247, Amazonia region in Peru,” Sydowia, vol. 71, pp. 17–24, 2019.
2017. [29] M. Corazon-Guivin, A. Cerna-Mendoza, and J. Guerrero-
[15] S. Ivanov, J. Austin II, R. H. Berg, and M. J. Harrison, Abad, “Nanoglomus plukenetiae, a new fungus from Peru, and
“Extensive membrane systems at the host-arbuscular mycor- a key to small-spored Glomeraceae species, including three
rhizal fungus interface,” Nature Plants, vol. 5, no. 2, pp. 194– new genera in the “Dominikia complex/clades”,” Mycological
203, 2019. Progress, vol. 18, pp. 1395–1409, 2019.
[16] P. Teotia, M. Kumar, R. Prasad, V. Kumar, N. Tuteja, and [30] M. Corazon-Guivin, A. Cerna-Mendoza, J. Guerrero-Abad,
A. Varma, “Mobilization of micronutrients by mycorrhizal A. Vallejos-Tapullima, G. Silva, and F. Oehl, “Acaulospora
fungi,” in Mycorrhiza—Function, Diversity, State of the Art, aspera, a new fungal species in the Glomeromycetes from
A. Varma, R. Prasad, and N. Tuteja, Eds., pp. 9–26, Springer, rhizosphere soils of the inka nut (Plukenetia volubilis L.) in
Cham, 2017. Peru,” Journal of Applied Botany and Food Quality, vol. 92,
[17] V. Säle, J. Palenzuela, C. Azcón-Aguilar et al., “Ancient pp. 250–257, 2019.
lineages of arbuscular mycorrhizal fungi provide little plant [31] M. Corazon-Guivin, A. Cerna-Mendoza, and J. Guerrero-
benefit,” Mycorrhiza, vol. 31, pp. 559–576, 2021. Abad, “Microkamienskia gen. nov. and Microkamienskia
[18] S. Stürmer, “A history of the taxonomy and systematics of peruviana, a new arbuscular mycorrhizal fungus from
arbuscular mycorrhizal fungi belonging to the phylum Western Amazonia,” Nova Hedwigia, vol. 109, no. 3-4,
Glomeromycota,” Mycorrhiza, vol. 22, pp. 247–258, 2012. pp. 355–368, 2019.
[19] E.-H. Lee, J.-K. Eo, K.-H. Ka, and A.-H. Eom, “Diversity of [32] J. Song, J.-F. Liang, M. Mehrabi-Koushki, I. Krisai-Greilhuber,
arbuscular mycorrhizal fungi and their roles in ecosystems,” and B. Ali, “Fungal systematics and evolution: FUSE 5,”
Mycobiology, vol. 41, no. 3, pp. 121–125, 2013. Sydowia, vol. 71, pp. 141–245, 2019.
[20] C. Thonar, A. Erb, and J. Jansa, “Real-time PCR to quantify [33] M. A. Corazon-Guivin, A. Cerna-Mendoza, J. C. Guerrero-
composition of arbuscular mycorrhizal fungal communities— Abad et al., “Paraglomus occidentale, a new arbuscular
marker design, verification, calibration and field validation,” mycorrhizal fungus from the sources of the Amazon river in
Molecular Ecology Resources, vol. 12, no. 2, pp. 219–232, Peru, with a key to the Paraglomeromycetes species,” Sydowia,
2011. vol. 72, pp. 85–94, 2020.
[21] P. Kohout, R. Sudová, and M. Janoušková, “Comparison of [34] M. A. Corazon-Guivin, A. Vallejos-Tapullima, A. M. de la
commonly used primer sets for evaluating arbuscular Sota-Ricaldi et al., “Acaulospora flava, a new arbuscular
mycorrhizal fungal communities: is there a universal mycorrhizal fungus from Coffea arabica and Plukenetia
solution?” Soil Biology and Biochemistry, vol. 68, pp. 482– volubilis plantations at the sources of the Amazon river in
493, 2014. Peru,” Journal of Applied Botany and Food Quality, vol. 94,
[22] T. Thapa, U. De, and B. Chakraborty, “Association and root pp. 116–123, 2021.
colonization of some medicinal plants with arbuscular [35] M. A. Corazon-Guivin, A. Vallejos-Tapullima, A. M. de la
mycorrhizal fung,” Journal of Medicinal Plants Studies, Sota-Ricaldi et al., “Acaulospora flavopapillosa, a new fungus
vol. 3, no. 2, pp. 25–35, 2015. in the Glomeromycetes from a coffee plantation in Peru, with
[23] M. Corazón-Guivin, A. Vallejos-Tapullima, and S. Rengifo- an updated key for the identification of Acaulosporaceae
Del Aguila, “Influence of substrate properties on communities species,” Journal of Applied Botany and Food Quality, vol. 95,
of arbuscular mycorrhizal fungi isolated from agroecosystems pp. 6–16, 2022.
8 Advances in Agriculture
[36] M. Corazón-Guivin, G. Vallejos-Torres, A. Vallejos-Tapullima Applied and Environmental Microbiology, vol. 87, no. 17,
et al., “Rhizoglomus cacao, a new species of the Glomeraceae from pp. 1–13, Article ID e0034921, 2021.
the rhizosphere of Theobroma cacao in Peru, with an updated [52] L. Wang, L. Zhang, T. S. George, and G. Feng, “A core
identification key for all species attributed to Rhizoglomus,” Nova microbiome in the hyphosphere of arbuscular mycorrhizal
Hedwigia, vol. 115, pp. 99–115, 2022. fungi has functional significance in organic phosphorus
[37] R. Lebeuf, A. Paul, Y. Lamoureux et al., “Fungal systematics mineralization,” New Phytologist, vol. 238, no. 2, pp. 859–873,
and evolution: FUSE 8,” Sydowia, vol. 74, pp. 193–249, 2022. 2023.
[38] R. Lebeuf, J. Landry, J. F. Ammirati et al., “Fungal systematics [53] S. Veresoglou, T. Caruso, and M. Rillig, “Modelling the
and evolution: FUSE 9,” Sydowia, vol. 75, pp. 313–377, 2023. environmental and soil factors that shape the niches of two
[39] F. Oehl, E. Sieverding, J. Palenzuela, K. Ineichen, and G. A. da common arbuscular mycorrhizal fungal families,” Plant and
Silva, “Advances in Glomeromycota taxonomy and classifica- Soil, vol. 368, pp. 507–518, 2013.
tion,” IMA Fungus, vol. 2, no. 2, pp. 191–199, 2011. [54] E. S. Coutinho, G. W. Fernandes, R. L. L. Berbara,
[40] J. Błaszkowski, M. Sanchez-Garcia, P. Niezgoda et al., “A new H. M. Valério, and B. T. Goto, “Variation of arbuscular
order, Entrophosporales, and three new Entrophospora species mycorrhizal fungal communities along an altitudinal gradient
in Glomeromycota,” Frontiers in Microbiology, vol. 13, pp. 1– in rupestrian grasslands in Brazil,” Mycorrhiza, vol. 25, no. 8,
25, 2022. pp. 627–638, 2015.
[41] N. N. Wijayawardene, K. D. Hyde, L. K. T. Al-Ani et al., [55] M. C. Arocha-Rodríguez, E. Pérez-Ortega, K. Fernández-
“Outline of fungi and fungus-like taxa,” Mycosphere, vol. 11, Suárez, and G. Haesaert, “Efecto del pH del medio de cultivo
no. 1, pp. 1060–1456, 2020. en el crecimiento presimbiótico de Rhizoglomus irregulare,”
[42] M. Krüger, H. Stockinger, C. Krüger, and A. Schüßler, “DNA- Cultivos Tropicales, vol. 40, pp. 1–12, 2019.
based species level detection of Glomeromycota: one PCR [56] L. C. Vieira, D. K. A. Silva, I. E. C. Escobar et al., “Changes in
primer set for all arbuscular mycorrhizal fungi,” New an arbuscular mycorrhizal fungi community along an
Phytologist, vol. 183, no. 1, pp. 212–223, 2009. environmental gradient,” Plants, vol. 9, no. 1, Article ID 52,
[43] H. Vierheilig, A. P. Coughlan, U. Wyss, and Y. Piché, “Ink and 2020.
vinegar, a simple staining technique for arbuscular- [57] A. Carrascosa, J. A. Pascual, A. López-García et al., “Different
mycorrhizal fungi,” Applied and Environmental Microbiology, functional and taxonomic composition of the microbiome in
vol. 64, no. 12, pp. 5004–5007, 1998. the rhizosphere of two purslane genotypes,” Agronomy,
[44] T. P. McGONIGLE, M. H. Miller, D. G. Evans, vol. 13, no. 7, Article ID 1795, 2023.
G. L. Fairchild, and J. A. Swan, “A new method which gives
an objective measure of colonization of roots by vesicular-
arbuscular mycorrhizal fungi,” New Phytologist, vol. 115,
no. 3, pp. 495–501, 1990.
[45] M. Bhuiyan, M. Banu, and M. Rahman, “Assessment of
arbuscular mycorrhizal association in some fruit and spice
plants of Rangamati hill district,” Bangladesh Journal of
Agricultural Research, vol. 42, no. 2, pp. 221–232, 2017.
[46] R. F. da Rui, S. C. Santos, E. R. P. Lourente, S. de Paula
Quintão Scalon, D. M. Dresch, and J. A. Schiavo, “Mudas de
Myrciaria glomerata (o. berg) com fungos micorrízicos
arbusculares e fósforo: crescimento e dependência micorrízica,”
in Tecnologia de Produção em Fruticultura, pp. 32–49, Atena
Editors, 2020.
[47] M. Öpik, A. Vanatoa, E. Vanatoa et al., “The online database
Maarj AM reveals global and ecosystemic distribution patterns
in arbuscular mycorrhizal fungi (Glomeromycota),” New
Phytologist, vol. 188, no. 1, pp. 223–241, 2010.
[48] K. Rojas-Mego, C. Elizarbe-Melgar, M. Gárate-Díaz, D. Ayala-
Montejo, R. Pedro, and E. Sieverding, “Hongos de micorriza
arbuscular en tres agroecosistemas de cacao (Theobroma cacao
L.) en la amazonía peruana,” Folia Amazónica, vol. 23, no. 2,
pp. 149–156, 2014.
[49] C. Peña-Venegas, G. Cardona, J. Arguelles, and A. L. Arcos,
“Micorrizas arbusculares del sur de la amazonia colombiana y
su relación con algunos factores fisicoquímicos y biológicos del
suelo,” Acta Amazónica, vol. 37, pp. 327–336, 2007.
[50] P. Ruiz, K. Rojas, and E. Sieverding, “La distribución geográfica
de los hongos de micorriza arbuscular: una prioridad de
investigación en la Amazonía peruana,” Espacio y Desarrollo,
vol. 1, no. 23, pp. 47–63, 2011.
[51] Y. Ma, H. Zhang, D. Wang et al., “Differential responses of
arbuscular mycorrhizal fungal communities to long-term
fertilization in the wheat rhizosphere and root endosphere,”