Revista Mexicana Ciencias Agrícolas   volume 12   number 4   May 16 - June 29, 2021

DOI: https://doi.org/10.29312/remexca.v12i4.2620

Article

Botryosphaeriaceae: a complex, diverse and cosmopolitan family of fungi

Alejandra Mondragón-Flores1, 2

Gerardo Rodríguez-Alvarado2

Nuria Gómez-Dorantes2

Jesús Jaime Guerra-Santos3

Sylvia Patricia Fernández-Pavía2§

1Valle de Apatzingán Experimental Field-INIFAP. Highway Apatzingán-Four roads km 17.5, Antúnez, Michoacán. CP. 60780. Tel. 800 0882222, ext. 84610. (mondragon.flores@gmail.com). 2Institute of Agricultural and Forestry Research-UMSNH. Highway Morelia-Zinapécuaro km 9.5, Tarímbaro, Michoacán. CP. 58880. Tel. 443 3223500, ext. 5226. (fernandezpavia@hotmail.com; gra.labpv@gmail.com; nuriah@live.com.mx). 3Autonomous University of Carmen-Faculty of Natural Sciences-Environmental Sciences Research Center. Laguna de Terms Street s/n, col. 2nd section renewal, Carmen City, Campeche, Mexico. CP. 24155. Tel. 938 1343965. (jjguerra-santos@hotmail.com).

§Corresponding author: fernandezpavia@hotmail.com.

Abstract

In the last decade, interest in studying the fungi belonging to the Botryosphaeriaceae family has increased due to the diseases that induce in economically important crops, their wide cosmopolitan distribution and the observed association between pathogenesis and host stress. More than ten species associated with symptoms in different parts of the same plant have been reported, indicating that a significant number of species of this family do not have specificity in host range. Besides, several studies have shown the ability of these fungi to ‘jump’ from their original native hosts to agricultural crops that are established in nearby areas, belonging to the same botanical family or to a different family. The objective of this research is to review morphological and molecular markers for taxonomic identification of species in the Botryosphaeriaceae family, their geographical distribution, range of agricultural host and developmental aspects for the disease including dispersal modes. The information presented may be useful in the etiology, identification and diagnosis of Botryosphaeriaceae species as well as the management of the diseases caused by them.

Keywords: hosts, stress, symptoms.

Reception date: January 2021

Acceptance date: March 2021

Introduction

The family Botryosphaeriaceae is represented by 23 genera of cosmopolitan fungi with a wide range of hosts and that can be endophytes, phytopathogenic or saprophytes (Slippers and Wingfield, 2007; Slippers et al., 2017). Members of this family induce diseases in plants that are under some form of stress (De Wet et al., 2003). They can cause symptoms such as cankers, gummosis, dieback of branches, defoliation and leaf necrosis and plant death; in general, all these symptoms are called decline syndrome (Slippers and Wingfield, 2007).

In recent years, unknown species have been described in various hosts in new geographical regions (Netto et al., 2017). This indicates that these fungi are dispersing around the world as a result of commercial globalization mainly, making them a potential threat to agroecosystems, forests, native and introduced plants (Slippers et al., 2017).

Identification of Botryosphaeriaceae species

The family Botryosphaeriaceae was introduced by Theissen and Sydow (1918) and belongs to the order Botryosphaeriales (Schoch et al., 2006). The genera that have a global geographical distribution and affect a greater number of hosts are Diplodia, Dothiorella, Lasiodiplodia and Neofusicoccum, encompassing 70%, with approximately 300 phytopathogenic species (Slippers et al., 2017).

The morphological characteristics of mycelium and asexual fruiting bodies are used for identification at the genus and species level (Alves et al., 2006; Sandoval-Sánchez et al., 2013). However, these characteristics are very variable and sometimes not distinctive, because they share between species; they are also influenced by age and substrate where isolates grow, therefore it is necessary to use molecular tools (Alves et al., 2007).

The sequences of genes that encode for elongation factor 1- α (TEF1- α), beta tubulin (β-Tub) and internal transcribed spacers (ITS) are the molecular regions most commonly used in phylogenetic analyses for the identification of Botryosphaeriaceae species (White et al., 1990; Alves et al., 2006; Zhou et al., 2015). Another gene that is also useful is the second largest subunit of RNA polymerase II (RPB2) (Fernández-Herrera et al., 2017).

Recently, Lopes and collaborators (2017) suggested that the genes MAT1-2-1 and MAT1-1-1 are efficient in resolution of species within the genus Neofusicoccum and were useful in demonstrating that most species are homothallic. One disadvantage of using these markers is that both genes cannot always be obtained or only one isolate of one species is available. The gen MAT1-2-1 is more accurate and reliable for species differentiation by containing fewer preserved introns and better PCR amplification is obtained.

Another tool for differentiating Botryosphaeriaceae species is the analysis through intern simple sequence repeat (ISSR), which is a simple, reproducible, fast and useful technique when it comes to sequencing a large number of isolates, grouping those of the same species, determining inter-specific variability and differentiating cryptic species as well as detecting intra-specific variability (Zhou et al., 2001).

Hybrid species, morphotypes and cryptic species complexes occupying the same ecological niche have been identified in the Botryosphaeriaceae family. In these cases, it is difficult to differentiate species when only one or two loci are used for identification (De Wet et al., 2003; Cruywagen et al., 2017). Multilocus analysis of DNA sequences and the use of more isolates in analyses is currently the most efficient way to recognize hybrid species, morphotypes and cryptic species complex (Cruywagen et al., 2017).

For efficient differentiation of morphotypes, De Wet et al. (2003) used the analysis of six coding genes of beta tubulin proteins (β-Tub), chitin synthetase (CHS), elongation factor 1-α (TEF1-α), actin (ACT), calmodulin (CAL) and glutaraldehyde-6-phosphate (GPD), as well as six microsatellite loci (SS5, SS7, SS8, SS9, SS10 and SS11).

Distribution

Slippers et al. (2017) indicate that phytopathogenic fungi belonging to Botryosphaeriaceae generally affect plants in subtropical and tropical zones, however, in recent years its presence has been reported worldwide, an example of the above are the species of Neofusicoccum that are known to colonize 46 hosts from 18 botanical families in ten countries including all continents (Sakadilis et al., 2011).

This ability to infect multiple hosts and migrate between them facilitates the establishment and spread of species and genotypes of Botryosphaeriaceae in new areas (Mehl et al., 2017). Some members of this family may have some specificity, which is influenced by the host and its habitat (Slippers and Wingfield, 2017). Human activities that influence phytopathogen dispersion and its interactions with its hosts are: the introduction of non-native plants in new areas, changes in land use and intensive deforestation (Pavlic-Zup et al., 2015).

In addition, when these fungi infect plants in conditions of high temperatures and drought, they can become very aggressive pathogens and result in a potential threat to agroecosystems, natural forests, native and introduced plants (Piskur et al., 2011). This has led to an increase in interest in studying these fungi due to their presence in multiple hosts, new geographical areas and their aggressiveness in hosts under stress (Slippers et al., 2017).

Host range

The phytopathogenic species of Botryosphaeriaceae attack woody plants (Sakalidis et al., 2011). They are considered to attack mainly angiosperms, although in the case of Diplodia species which are restricted to gymnosperms, it has been suggested that it comes from an ancestor of Botryosphaeriaceae that evolved in angiosperms (De Wet et al., 2008). There are studies that demonstrate the ability of these fungi to move from native to non-native hosts and between plants close or distant phylogenetically (Sakadilis et al., 2013; Pavlic-Zup et al., 2015).

Some of the new species that have been identified are restricted to a single host and are not very pathogenic, suggesting that they are recently introduced or that they are only associated endophytically (Perez et al., 2010). However, cases of host infected by only one or more than ten species associated with symptoms in different parts of the plant have been reported, indicating that they can infect more than one organ indistinctly (Delgado-Cerrone et al., 2016; Mayorquin et al., 2016; Tedihou et al., 2017).

Some authors indicate that the most frequently isolated species in a host is usually not the most aggressive (Mayorquin et al., 2016). Due to the lack of consistency to delimit Botryiosphaeria species, it is difficult to quantify how many plants they attack, however, in a recent study approximately 1 692 hosts worldwide were determined (Batista et al., 2012). These pathogens attack ornamental forest plants and various agricultural hosts, including tropical fruit trees (Fernández-Herrera et al., 2017; Lawrence et al., 2017) (Table 1), deciduous shrubs, herbaceous plants and palms (Table 2).

Table 1. Distribution of Botryosphaeriaceae species associated with canker, gummosis, decline and rot in evergreen fruit trees.

*= species described recently.

Table 2. Distribution of Botryosphaeriaceae species associated with canker, gummosis, decline and rot in shrub, deciduous, herbaceous and palm hosts.

*= species described recently.

Factors that condition the disease

The phytopathogenic species of Botryosphaeriaceae have a great diversity of hosts, are opportunistic fungi capable of colonizing a large number of botanical species and causing disease in those that are under some type of stress, mainly water stress (De Wet et al., 2003). This could be explained because in response to the lack of water, the plant increases levels of abscisic acid and its defenses regulated by jasmonic acid, ethylene and salicylic acid are suppressed and as a result susceptibility to pathogens is increased (Asselbergh et al., 2008).

This is important given the emerging climate change conditions that not only increases stress in plant communities but also promotes pathogen development and their survival rates (Slippers and Wingfield, 2017). Stress in plants modifies their susceptibility to pathogens which causes changes in the impact of diseases on crops (Elad and Pertot, 2014).

Symptoms

Diseases of consideration in various crops of agricultural importance are associated with members of Botryosphaeriaceae (Eskalen et al., 2013; Bautista-Cruz et al., 2018). Some studies carried out by Rosado et al. (2016) indicate that often multiple species of the same genus, as well as different genera, are associated with the symptoms and it is difficult to differentiate them for each species (Delgado-Cerrone et al., 2016). 

In some cases, it has been possible to associate symptoms with the pathogen species due to certain characteristics such as the presence of rings in injuries (Tian et al., 2018). Symptoms associated with these fungi are: canker in branches and trunk, decline, gummosis, dieback of branches, necrosis in leaves, rots of seeds, fruits, peduncle, root and blight of shoots and inflorescences (Slippers et al., 2005; Sandoval-Sánchez et al., 2013; Dugan et al., 2015; Hajlaoui et al., 2015; Netto et al., 2017; Rodríguez-Gálvez et al., 2017). 

Transmission and dispersion

According to Bihon et al. (2011), these fungi are transmitted horizontally from mature plants to young plants by means of spores; however, vertical transmission has not yet been proven. The release of spores is more frequent during the rainy period than in other seasons, and these are mainly dispersed by splashing rainwater (Skalen et al., 2013). 

Research indicates that in addition to their potential as pathogens, they can be associated with fungi of other families and transmitted by bark beetle (Hypocryphalus mangiferae), which acts as a vector in the dispersion between hosts (Adawi et al., 2006). On the other hand, it is believed that the dieback caused by these fungi could serve as a mitigating of other major diseases such as the sudden oak death, by killing branches that would otherwise produce leaves that easily become infected with Phytophthora ramorum and that are spread through splashes of rainwater (Lawrence et al., 2017).

When fruit trees are subjected to cultural practices, pruning wounds are a source of stress for the plant and provide an entry point to pathogens that colonize tissues in a basipetal form (Rodríguez-Gálvez et al., 2017). There are reports that indicate that the presence of a wound is not necessary for fungi to infect the host’s organs, however, they do contribute to increasing the severity of symptoms (Zhou et al., 2015).

Abiotic factors such as the increase of temperature, high relative humidity, droughts, frosts, high planting densities and poor pruning practices favor the development of the disease increasing the incidence that ranges from 20 to 97% in some crops (De la Mora-Castañeda et al., 2014; Fernández-Herrera et al., 2017; Bautista-Cruz et al., 2018).

Conclusions

The Botryosphaeriaceae family is of great importance for the diseases that cause in crops of agricultural importance in all temperate, tropical and subtropical areas around the world. Their ability to move from endophyte to pathogen in plants under stress means a threat in crops subjected to suboptimal developmental conditions, water stress, for example.

Due to the lack of information on aspects of reproduction, survival, dispersion and accurate detection and identification techniques, more studies on these pathogens to establish appropriate disease control and management measures are required globally.

Cited literature

Abdollahzadeh, J.; Javadi, A.; Goltapeh, M. E.; Zare, R. and Phillips, A. J. L. 2010. Phylogeny and morphology of four new species of Lasiodiplodia from Iran. Persoonia. 25(10):1-10. Doi: 10.3767/003158510X524150.

Adesemoye, A. O. and Eskalen, A. 2011. First report of Spencermartinsia viticola, Neofusicoccum australe and N. parvum causing branch canker of citrus in California. Plant Dis. 95(6):770. https://doi.org/10.1094/PDIS-02-11-0092.

Adesemoye, A. O.; Mayorquin, J. S.; Wang, D. H.; Twizeyimana, M.; Lynch, S. C. and Eskalen, A. 2014. Identification of species of Botryosphaeriaceae causing bot gummosis in citrus in California. Plant disease. 98(1):55-61. Doi: 10.1094/PDIS-05-13-0492-RE.

Al-Adawi, A. O.; Deadman, M. L.; Al-Rawahi, A. K.; Al-Maqbali, Y. M.; Al-Jahwari, A. A.; Al-Saadi, B. A.; Al-Amri, I. S. and Wingfield, M. J. 2006. Etiology and causal agents of mango sudden decline disease in the Sultanate of Oman. Eur. J. Plant Pathol. 116(4):247-254. Doi: 10.1007/s10658-006-9056-x.

Al-Sadi, A. M.; Al-Wehaibi, A. N.; Al-Shariqi, R. M.; Al-Hammadi, M. S.; Al-Hosni, I. A.; Al-Mahmooli, I. H. and Al-Ghaithi, A. G. 2013. Population genetic analysis reveals diversity in Lasiodiplodia species infecting date palm, citrus, and mango in oman and the UAE. Plant Disc. 97(10):1363-1369. Doi: 10.1094/PDIS-03-13-0245-RE.

Alves, A.; Correia, A. and Phillips, A. J. L. 2006. Multi-gene genealogies and morphological data support Diplodia cupressi sp. nov., previously recognized as D. pinea f. sp. cupressi, as a distinct species. Fungal Diversity. 23(1):1-15.

Alves, A.; Phillips, A. J. L.; Henriques, I. and Correia, A. 2007. Rapid differentiation of species of botryosphaeriaceae by PCR fingerprinting. Res. Microbiol. 158(2):112-121. https://doi.org/10.1016/j.resmic.2006.10.003.

Asselbergh, B.; De-Vleesschauwer, D. and Höfte, M. 2008. Global switches and fine- tuning ABA modulates plant pathogen defense. Mol. Plant Microbe Interact. 21(6):709-719. Doi: 10.1094/MPMI-21-6-0709.

Avilés, M.; Castillo, S.; Bascon, J.; Zea Bonilla, T.; Martín‐Sánchez, P. M. and Pérez‐Jiménez, R. M. 2008. First report of Macrophomina phaseolina causing crown and root rot of strawberry in Spain. Plant Pathol. 57(2):382-382. Doi: 10.1111/j.1365-3059.2007.01717.x.

Awan, Q. N.; Akgül, D. S. and Unal, G. 2016. First Report of Lasiodiplodia pseudotheobromae causing postharvest fruit rot of lemon in Turkey. Plant Disc. 100(11):2327. Doi: 10.1094/PDIS-04-16-0512-PDN. 

Batista, E.; Lopes, A. and Alves, A. 2012. What do we know about Botryosphaeriaceae? an overview of a worldwide cured dataset. Forests. 12(3):313. https://doi.org/10.3390/ f12030313.

Bautista-Cruz, M. A.; Almaguer-Vargas, G.; Leyva-Mir, S. G.; Colinas-León, M. T.; Correia, K. C.; Camacho-Tapia, M.; Robles-Yerena, L.; Michereff, S. J. and Tovar-Pedraza, J. M. 2018. Phylogeny, distribution, and pathogenicity of Lasiodiplodia species associated with cankers and dieback symptoms of persian lime in Mexico. Plant Dis. 103(6):1156-1165. Doi: 10.1094/PDIS-06-18-1036-RE.

Billones-Baaijens, R.; Ridgway, H. J.; Jones, E. E. and Jaspers, M. V. 2015. Spatial distribution of Neofusicoccum species within a rootstock mother vine indicates potential infection pathways. Eur. J. Plant Pathol. 141(2):267-279. Doi: 10.1007/s10658-014-0540-4.

Bihon, W.; Slippers, B.; Burgues, T.; Wingfield, M. J. and Wingfield, B. D. 2011. Sources of Diplodia pinea endophytic infections in Pinus patula and P. radiata seedlings in South Africa. Forest Pathol. 41(5):370-375. Doi: 10.1111/j.1439-0329.2010.00691.x.

Boyzo-Marin, J.; Rebollar-Alviter, A.; Silva-Rojas, H. V. and Ramirez-Maldonaldo, G. 2016. First report of Neofusicoccum parvum causing stem blight and dieback of blueberry in Mexico. Plant Dis. 100(12):2524-2524. https://doi.org/10.1094/PDIS-02-17-0251-PDN.

Contreras-Pérez, M.; Santoyo-Pizano, G.; De los Santos-Villalobos, S.; Gutiérrez-García, M. A.; Orozco-Mosqueda, M. C. and Rocha-Granados, M. C. 2019. First report of Lasiodiplodia on blackberry plants (Rubus subgenus Eubatus) in the Michoacan state, Mexico. Mex. J. Phytopathol. 37(3):479-485. Doi: 10.18781/R.MEX.FIT.1905-4.

Cruywagen, E. M.; Slippers, B.; Roux, J. and Wingfield, M. J. 2017. Phylogenetic species recognition and hybridisation in Lasiodiplodia: a case study on species from baobabs. Fungal Biol. 121(4):420-436. Doi: 10.1016/j.funbio.2016.07.014.

Delgado-Cerrone, L.; Mondino-Hintz, P. and Alaniz-Ferro, S. 2016. Botryosphariaceae species associated with stem canker, die-back and fruit rot on apple in Uruguay. Eur. J. Plant Pathol. 146(3):637-655. Doi: 10.1007/s10658-016-0949-z.

De-Wet, J.; Burguess, T.; Slippers, B.; Preisig, O.; Wingfield, B. D. and Wingfield, M. J. 2003. Multiple gene genealogies and microsatellite markers reflect relationships between morphotypes of Sphaeropsis sapinea and distinguish a new species of Diplodia. Mycol. Res. 107(5):557-566. https://doi.org/10.1017/S0953756203007706.

De-Wet, J.; Slippers, B.; Preisig, O.; Wingfield, B. D. and Wingfield, M. J. 2008. Phylogeny of the Botryosphaeriaceae reveals patterns of host association. Mol. Phylogen. Evol. 46(1):116-126. Doi: 10.1016/j.ympev.2007.08.016.

Dugan, F. M.; Lupien, S. L.; Osuagwu, A. N.; Uyoh, E. A.; Okpako, E. and Kisha, T. 2015. New records of Lasiodiplodia theobromae in seed of Tetrapleurra tetraptera form Nigeria and fruit of Cocos nucifera from Mexico. J. Phytopathol. 164(1):65-68. Doi: 10.1111/JPH.12384.

Eland, Y. and Pertot, I. 2014. Climate change impacts on plant pathogens and plant diseases. J.  Crop Improv. 28(1):99-139. Doi: 10.1080/15427528.2014.865412.

Eskalen, A.; Faber, B. and Bianchi, M. 2013. Spore trapping and pathogenicity of fungi in the Botryosphaeriaceae and Diaporthaceae associated with avocado branch canker in California. Plant Dis. 97(3):329-332. Doi: 10.1094/PDIS-03-12-0260-RE.

Fernández-Herrera, E.; Moreno-Salazar, S.; Rentería-Martínez, M. E.; Arratia-Castro, A. A. and Villar-Luna, E. 2017. Neoscytalidium dimidiatum: causal agent of dieback in Ficus benjamina L. in Mexico. Rev. Chapingo. Ser. Hortic. 23(3):203-210. Doi: 10.5154/r.rchsh.2017.02.009.

Guajardo, J.; Riquelme, N.; Tapia, L.; Larach, A.; Torres, C.; Camps, R. and Besoain, X. 2018. First report of Lasiodiplodia theobromae causing bot gummosis in Citrus limon in Chile. Plant Dis. 102(4):818. DOI: 10.1094/PDIS-09-17-1517-PDN.

Hajlaoui, M. R.; Mnari-Hattab, M.; Sayen, M.; Zarrouk, I.; Jemmali, A. and Koike, S. T. 2015. First report of Macrophomina phaseolina causing charcoal rot of strawberry in Tunisia. New Dis. Rep. 32(1):14. Doi: 10.5197/j.2044-0588.2015.032.014.

Hilário, S.; Lopes, A.; Santos, L. and Alves, A. 2019. Botryosphaeriaceae species associated with blueberry stem blight and dieback in the centre region of portugal. Eur. J. Plant Pathol. 156(3):31-44. Doi: 10.1007/s10658-019-01860-6.

Ismail, A. M.; Cirvilleri, G.; Polizzi, G.; Crous, P. W.; Groenewald, J. Z. and Lombard, L. 2012. Lasiodiplodia species associated with dieback disease of mango (Mangifera indica) in egypt. Australasian Plant Pathol. 41(6):649-660. https://doi.org/10.1007/s13313-012-0163-1.

Lawrence, P.; Peduto, H. F.; Gubler, W. D. and Trouillas, F. P. 2017. Botryosphaeriaceae species associated with dieback and canker disease of bay laurel in northern California with the description of Dothiorella californica sp. nov. Fungal Biol. 121(4):347-360. Doi: 10.1016/j.funbio.2016.09.005.

Leyva-Mir, S. G.; Velázquez-Martínez, G. C.; Tlapal-Bolaños, B.; Tovar-Pedraza J. M.; Rosas-Salto, G. H. y Alvarado-Gómez, O. G. 2015. Caracterización morfológica y molecular de aislados de Macrophomina phaseolina asociados a caña de azúcar en México. Rev. Argentina Microbiol. 47(2):143-147. https://doi.org/10.1016/j.ram.2015.03.003.

Lopes, A.; Phillips, A. J. L. and Alves, A. 2017. Mating type genes in the genus Neofusicoccum: Mating strategies and usefulness in species delimitation. Fungal Biol. 121(4):394-404. Doi: 10.1016/j.funbio.2016.08.011.

Mayorquin, J. S.; Wang, D. H.; Twizeyimana, M. and Eskalen, A. 2016. Identification, distribution, and pathogenicity of Diatrypaceae and Botryosphaeriaceae associated with citrus branch canker in the southern California desert. Plant Dis. 100(12):2402-2413. Doi: 10.1094/PDIS-03-16-0362-RE.

Mc-Donald, V. and Eskalen, A. 2011. Botryosphaeriaceae species associated with avocado branch canker in California. Plant Dis. 95(11):1465-1473. Doi: 10.1094/PDIS-02-11-0136.

Mehl, J. W. M.; Slippers, B.; Roux, J. and Wingfield, M. J. 2017. Overlap of latent pathogens in the Botryosphaeriaceae on a native and agricultural host. Fungal Biol. 121(4):405-419. Doi: 10.1016/j.funbio.2016.07.015.

Molina-Gayosso, E.; Silva-Rojas, H. V.; García-Morales, S. and Ávila-Quezada, G. 2012. First report of black spots on avocado fruit caused by Neofusicoccum parvum in Mexico. Plant Dis. 96(2):287. Doi: 10.1094/PDIS-08-11-0699.

Modragón-Flores, A.; López-Medina, J.; Ochoa-Ascencio, S. y Gutiérrez-Contreras, M. 2012. Hongos asociados a la parte aérea del arándano en Los Reyes, Michoacán, México. Rev. Mex. Fitopatol. 30(2):141-144.

Netto, M. S. B.; Assunção, I. P.; Lima, G. S. A.; Marques, M. W.; Lima, W. G.; Monteiro, J. H. A.; Balbino, V. Q.; Michereff, S. J.; Phillips, A. J. L. and Câmara, M. P. S. 2014. Species of Lasiodiplodia associated with papaya stem-end rot in Brazil. Fungal Divers. 67(1):127-141. Doi: 10.1007/s13225-014-0279-4.

Netto, M. S. B.; Lima, W. G.; Correia, K. C.; Da Silva, CH. F. B.; Thon, M.; Martins, R. B.; Miller, R. N. G.; Michereff, S. J. and Camara, M. P. S. 2017. Analysis of phylogeny, distribution, and pathogenicity of Botryosphaeriaceae species associated with gummosis of anacardium in Brazil, with a new species of Lasiodiplodia. Fungal Biol. 121(4):437-451. Doi: 10.1016/j.funbio.2016.07.006.

Pavlic-Zup, D.; Wingfield, M. J.; Boissin, E. and Slippers, B. 2015. The distribution of genetic diversity in the Neofusicoccum parvum/N. ribis complex suggests structure correlated with level of disturbance. Fungal Ecol. 13(13):93-102. Doi: 10.1016/j.funeco.2014.09.002.

Pérez, C. A.; Wingfield, M. J.; Slippers, B.; Altier, N. A. and Blanchette, R. A. 2010. Endophytic and canker-associated Botryosphaeriaceae occurring on non-native eucalyptus and native myrtaceae trees in Uruguay. Fungal Divers. 41(1):53-69. Doi: 10.1007/s13225-009-0014-8.

Pis-kur, B.; Pavlic, D.; Slippers, B.; Ogris, N.; Maresi, G.; Wingfield, M. J. and Jurc, D. 2011. Diversity and pathogenicity of Botryosphaeriaceae on declining Ostrya carpinifolia in Slovenia and Italy following extreme weather conditions. Eur. J. Forest Res. 130(2):235-249. Doi: 10.1007/s10342-010-0424-x.

Polanco-Florián, L. G.; Alvarado-Gómez, O. G.; Pérez-González, O.; González-Garza, R. y Olivares-Sáenz, E. 2019. Hongos asociados con la muerte regresiva de los cítricos en Nuevo León y Tamaulipas, México. Rev. Mex. Cienc. Agríc. 10(4):757-764. Doi: 10.29312/remexca.v10i4.1417.

Polizzi, G.; Aiello, D.; Vitale, A.; Giuffrida, F.; Groenewald, J. Z. and Crous P. W. 2009. First report of shoot blight, canker, and gummosis caused by Neoscytalidium dimidiatum on citrus in Italy. Plant Dis. 93(11):1215-1215. Doi: 10.1094/PDIS-93-11-1215A.

Rodríguez-Gálvez, E.; Guerrero, P.; Barradas, C.; Crous, P. W. and Alves, A. 2017. Phylogeny and pathogenicity of Lasiodiplodia species associated with dieback of mango in Peru. Fungal Biol. 121(4):452-465. Doi: 10.1016/j.funbio.2016.06.004.

Sakalidis, L. M.; Hardy, G. E. S. J. and Burgess, T. I. 2011. Class III endophytes, clandestine movement amongst hosts and habitats and their potential for disease; a focus on Neofusicoccum austral. Australasian Plant Pathol. 40(5):510-521. Https://doi.org/10.1007/s13313-011-0077-3.

Sakalidis, M. L.; Slippers, B.; Wingfield, B. D.; Hardy, G. E. S. J. and Burgess T. I. 2013. The challenge of understanding the origin, pathways and extent of fungal invasions: global populations of the Neofusicoccum parvum/N. ribis species complex. Divers. Distrib. 19(8):873-1094. Doi: 10.1111/DDI.12030.

Sánchez, S.; Gambardella, M.; Henríquez, J. L. and Díaz I. 2013. First report of crown rot of strawberry caused by Macrophomina phaseolina in Chile. Plant Dis. 97(7):996. Doi: 10.1094/PDIS-12-12-1121-PDN.

Sandoval-Sánchez, M.; Nieto-Ángel, D.; Sandoval-Islas, J.; Téliz-Ortiz, D.; Orozco-Santos, M. y Silva-Rojas, H. V. 2013. Hongos asociados a pudrición del pedúnculo y muerte descendente del mango (Mangifera indica L.). Agrociencia. 47(1):61-73.

Schoch, C. L.; Shoemaker, R. A.; Seifert, K. A.; Hambleton, S.; Spatafora, J. W. and Crous, P. W. 2006. A multigene phylogeny of the dothideomycetes using four nuclear loci. Mycologia. 98(6):1041-1052. Doi: 10.3852/mycologia.98.6.1041.

Serret-López, R. E.; Tlapal-Bolaños, B.; Leyva-Mir, S. G.; Correia, K. C.; Camacho-Tapia, M.; Méndez-Jaimes, F. and Tovar-Pedraza, J. M. 2017. First report of Neofusicoccum algeriense causing dieback of red raspberry in Mexico. Plant Dis. 101(9):1673-1673. https://doi.org/10.1094/PDIS-02-17-0251-PDN.

Serrato-Diaz, L. M.; Aviles-Noriega, A.; Soto-Bauzo, A.; Rivera-Vargas, L. I.; Goenaga, R. and Bayman, P. 2019. Botryosphaeriaceae fungi as causal agents of dieback and corky bark in rambutan and Longan. Plant Dis. 104(1):105-115. Doi: 10.1094/PDIS-02-19-0295-RE.

Slippers, B.; Crous, P. W.; Jami F.; Groenewald, J. Z. and Wingfield, M. J. 2017. Diversity in the botryosphaeriales: looking back, looking forward. Fungal Biol. 121(4):307-321. Doi: 10.1016/j.funbio.2017.02.002.

Slippers, B.; Johnson, G. I.; Crous, P. W.; Coutinho, T. A.; Wingfield, B. D. and Wingfield, M. J. 2005. Phylogenetic and morphological re-evaluation of the Botryosphaeria species causing diseases of Mangifera indica. Mycologia. 97(1):99-110. Doi: 10.3852/mycologia.97.1.99.

Slippers, B. and Wingfield, M. J. 2007. Botryosphaeriaceae as endophytes and latent pathogens of woody plants: diversity, ecology and their impact. Fungal Biol. Rev. 21(2-3):90-106. Doi: 10.1016/j.fbr.2007.06.002.

Tedihou, E.; Kpemoua, K. and Tounou, A. 2017. Dépérissement des manguiers et citrus dans la région centrale du togo et méthodes de lutte par des fongicides. J. Appl. Bioscience. 119(1):11829-11838. Doi: 10.4314/jab.v119i1.1.

Theissen, F. and Sydow, H. 1918. Vorentwürfe zu den pseudosphaeriales. Annales Mycol. 16(1-2):1-34.

Tian, Y.; Zhao, Y.; Sun, T. and Wang, L. 2018. Identification and characterization of Phomopsis amygdali and Botryosphaeria dothidea associated with peach shoot blight in yangshan, China. Plant Dis. 102(12):2511-2518. Doi: 10.1094/PDIS-02-18-0243-RE.

Tovar-Pedraza, J. M.; Mora-Aguilera, J. A.; Nava-Díaz, C.; Téliz-Ortíz, D.; Valdovinos-Ponce, G.; Villegas-Monter, Á. y Hernández-Morales, J. 2012. Identificación, patogenicidad e histopatología de Lasiodiplodia theobromae en injertos de zapote mamey en Guerrero, México. Agrociencia. 46(2):147-161.

Trakunyingcharoen, T.; Cheewangkoon, R.; To-anun, C.; Crous, P. W.; Van Niekerk, J. M. and Lombard, L. 2014. Botryosphaeriaceae associated with diseases of mango (Mangifera indica). Australasian Plant Pathol. 43(4):425-438. Doi: 10.1007/s13313-014-0284-9.

Valencia, A. L.; Gil, P. M.; Latorre, B. A. and Rosales, I. M. 2019. Characterization and pathogenicity of Botryosphaeriaceae species obtained from avocado trees with branch canker and dieback and from avocado fruit with stem end rot in Chile. Plant Dis. 103(5):996-1005. Doi: 10.1094/PDIS-07-18-1131-RE.

Valle-De la Paz, M.; Guillén-Sánchez, D.; Perales-Rosas, D.; López-Martínez, V.; Juárez-López, P.; Martínez-Fernández, E.; Hernández-Arenas, M.; Ariza-Flores, R. and Gijón-Hernán, A. R. 2019. Distribution, incidence and severity of dieback (Lasiodiplodia spp.) in persa lime in Morelos, Mexico. Mex. J. Phytopathol. 37(3):464-478. Doi: 10.18781/R.MEX.FIT. 1904-7.

Wang, F.; Zhao, L.; Li, G.; Huang, J. and Hsiang, T. 2011. Identification and characterization of Botryosphaeria spp. causing gummosis of peach trees in Hubei province, central China. Plant Dis. 95(11):1378-1384. Doi: 10.1094/PDIS-12-10-0893.

Xu, Ch.; Zhang, H.; Zhou, Z.; Hu, T.; Wang, S.; Wang, Y. and Cao, K. 2015. Identification and distribution of Botryosphaeriaceae species associated with blueberry stem blight in China. Eur. J. Plant Pathol. 143(4):737-752. Doi: 10.1007/s10658-015-0724-6.

Xue, D.; Meng, L.; Li, G.; Li, B. and Wang, C. 2019. First report of Lasiodiplodia pseudotheobromae causing canker and shoot dieback on apple in China. Plant Dis. 103(9):2478. https://doi.org/10.1094/PDIS-01-19-0182-PDN.

Zhang, W. and Niu, X. L. 2019. First report of Lasiodiplodia theobromae causing postharvest stem end rot on coconut in China. Plant Dis. 103(6):1420-1420. https://doi.org/10.1094/PDIS-10-18-1861-PDN.

Zhai, L.; Zhang, M.; Lv, G.; Chen, X.; Jia, N.; Hong, N. and Wang, G. 2014. Biological and molecular characterization of four Botryosphaeria species isolated from pear plants showing stem wart and stem canker in China. Plant Dis. 98(6):716-726. Doi: 10.1094/PDIS-10-13-1060-RE.

Zhou, Y.; Gong, G.; Cui, Y.; Zhang, D.; Chang, X.; Hu, R.; Liu, N. and Sun, X. 2015. Identification of Botryosphaeriaceae species causing kiwifruit rot in Sichuan province, China. Plant Dis. 99(5):699-708. https://doi.org/10.1094/PDIS-07-14-0727-RE.

Zhou, S.; Smith, D. R. and Stanosz, G. R. 2001. Differentiation of Botryosphaeria species and related anamorphic fungi using inter simple or short sequence repeat (ISSR) fingerprinting. Mycol. Res. 105(8):919-926. https://doi.org/10.1016/S0953-7562(08)61947-4.