Grape Ripe Rot Caused by the Colletotrichum Complex: Comparison
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Grape ripe rot, which is predominantly caused by the Colletotrichum species, presents a growing threat to global grape cultivation. This threat is amplified by the increasing populations of the Colletotrichum species in response to warmer climates.

  • grape ripe rot
  • Colletotrichum gloeosporioides species complex
  • infection process

1. Introduction

Grapes (Vitis spp.) are extensively cultivated worldwide, and they have considerable global importance and economic impact. The global vineyard area was estimated to be approximately 7.3 Mha in 2021. Over half of worldwide grape production contributes to the winemaking industry, with the remainder mainly used as table grapes, dried grapes, and the production of musts and juices [1]. However, this substantial industry encounters significant threats from fruit diseases that affect the grape’s berries, such as bitter rot, black rot, Botrytis bunch rot, and—notably—ripe rot [2,3][2][3].
Ripe rot is particularly adapted to warm, humid, subtropical climates, and it poses a significant threat to grape cultivation, especially across South and North America, Australasia, and Asia—including Brazil, the United States, Australia, Taiwan, Japan, Korea, and China [4,5,6,7,8,9,10][4][5][6][7][8][9][10]. It has been responsible for losses exceeding 30%, and, in some cases, up to 60% or even more [4,11,12][4][11][12]. This disease not only reduces grape yields, but also adversely affects the chemical composition and quality of grapes and wine, leading to off flavors and a brownish color [13,14,15,16][13][14][15][16].

2. Grape Ripe Rot Caused by the Colletotrichum Complex

Colletotrichum, recognized for its role in causing ripe rot in grapes and for affecting many other plants, is ranked among the top ten plant fungal pathogens [2,17,18][2][17][18]. C. gloeosporioides (Penz.) Penz. & Sacc. and C. acutatum J.H. Simmonds ex J. H. Simmonds are the major species within this context [18,19][18][19]. The early classification of the Colletotrichum species primarily relied on features such as colony morphology, conidial shape and size, appressoria, physiological characteristics, and the host plant [20,21][20][21]. This led to significant ambiguity, as some strains identified as the same species based on the morphology exhibited, or due to different pathogenicity or physiological characteristics; thus, this made Colletotrichum a catalog of confusion [17,22][17][22]. Since 2012, the introduction of multilocus sequence analysis (MLSA) has marked a prominent development in the field. MLSA employs an array of loci, including act, chs-1, gadph, tub2, his3, cal, tef, gs, sod2, and ITS, among others, for delineating species within this genus. This approach has facilitated the reclassification of the genus into at least 15 complexes, encompassing a total of 257 species [17,23,24,25][17][23][24][25]. These include the CGSC, the C. acutatum species complex (CASC), and others. Moreover, the ApMat locus demonstrated notable utility in distinguishing species within the CGSC, even when used alone [26,27][26][27]. Notably, pre-2012 studies (which often lack multigene analysis) should be interpreted with caution. When referring to a species complex such as C. gloeosporioides and C. acutatum without clear molecular evidence, the term sensu lato (s.l.; in a broad sense) is usually included for clarification. On the other hand, sensu stricto (s.s.; in a narrow sense) is used for the species that have been identified through MLSA or ApMat marker analysis. First identified in the United States in 1891, grape ripe rot was originally linked to C. gloeosporioides s.l. [28]. As research progressed, C. acutatum s.l. was also found to be a potential causative agent of this disease [6,7,10,29][6][7][10][29]. Today, grape ripe rot is understood to be triggered by a blend of the Colletotrichum species, predominantly from the CGSC and CASC, with occasional involvement from the C. boninense and C. orchidearum species complexes (Table 1).
Table 1.
List of the
Colletotrichum
species documented as causing grape ripe rot.
Colletotrichum

Species Complex		 Species Country/

Region		 Reference
C. gloeosporioides complex C. aenigma China [30,31][30][31]
  Japan [32] 2
  South Korea [33] 3
  USA [4,12][4][12] 2
  C. fructicola Brazil [5]
    China [9,31][9][31]
    Japan [34] 2
    Taiwan [35]
    USA [4] 2
  C. gloeosporioides s.s. China [9]
    USA [12] 2
    Japan [34]
  C. hebeiense China [30]
  C. kahawae Brazil [5]
    USA [12] 2
  C. perseae Japan [34]
  C. siamense Brazil [36]
    USA [4] 2
  C. tropicale Taiwan [35,37][35][37]
  C. viniferum Brazil [5]
    China [9,30,38][9][30][38]
    Japan [32,34][32][34] 2
    South Korea [39]
    Taiwan [8,40][8][40]
  C. viniferum-like species (Clade V) 1 Japan [34]
  Other C. gloeosporioides s.l. Australia [6,16][6][16]
    Thailand [41] 3
C. acutatum complex C. citri China [38]
C. fioriniae 1 USA [4,11,12][4][11][12]
  C. godetiae Italy [42]
  C. limitticola Brazil [5]
  C. nymphaeae Brazil [5]
    USA [12] 2
  C. pseudoacutatum China [31]
  Other C. acutatum s.l. Australia [6,16,31,[16][3143][6]][43]
    Japan [10,44][10][44]
    South Korea [7] 2
C. boninense complex C. karstii Brazil [5]
C. orchidearum complex C. cliviicola (syn. C. cliviae)-like species China [38]
1 Although the pathogenicity of these Colletotrichum species on grape berries still awaits confirmation through Koch’s postulates, these pathogens are considered the dominant species that cause ripe rot in their respective regions according to related references. Additionally, virulence tests via artificial inoculation have indicated significant pathogenicity. Due to these considerations, they are included in this table. 2 While the referenced article reported an isolation from grape berries, Koch’s postulates were not fulfilled in terms of definitively establishing its pathogenicity on berries. However, it is included in this table due to its established role in causing grape ripe rot or because the virulence tests via artificial inoculation that were reported in the reference indicate significant pathogenicity. 3 While labeled as anthracnose in the original report, the symptoms described are consistent with ripe rot, and are characterized by berry-rot-type manifestations.
The CGSC and CASC demonstrate significant divergence in multiple aspects, including not only temperature requirements, infection rates, spore dispersal, and fungicide sensitivity [6,45,46,47,48][6][45][46][47][48], but also geographical prevalence. For instance, various CASC members that are implicated in grape rot in America and Australia are notably absent in Asia, while C. viniferum L.J. Peng, L. Cai, K.D. Hyde & Z.Y. Liu, (a member of the CGSC), causes severe infections in parts of South America and Asia, but it is scarcely documented in other regions (Table 1). From a geographical perspective, CGSC is commonly found in warmer climates and CASC in cooler environments [12,19,49][12][19][49]. In the context of climate change and rising temperatures, regions previously unaffected by grape ripe rot may increasingly be confronted by the disease. Specifically, the warm-climate-preferring CGSC might become more prevalent in regions experiencing elevated temperatures. Furthermore, areas previously free of this disease could start facing encounters with ripe rot, either influenced by CGSC or induced by the cooler-environment-preferring CASC. Despite acknowledging the crucial role of both CGSC and CASC in the complex nature of grape ripe rot, this text primarily focus on CGSC owing to its significant influence in subtropical regions and its broader global distribution.

3. Diverse Grapevine Symptoms Caused by the CGSC

A wide array of symptoms on berries, flowers, and other vegetative tissues of grapevine can be attributed to species within the Colletotrichum genus and CGSC depending on their virulence and complicated interactions with various factors. Ripe rot typically manifests as a berry-rot type, beginning with lesions that evolve into dark, sunken necrotic spots with concentric rings that produce acervuli (asexual fruiting bodies of the pathogen). Upon exposure to moist conditions, the lesion surfaces proliferate into orange- or salmon-colored conidial masses, and ultimately result in the drying and mummification of decaying berries. While the symptoms on berries are relatively similar across different species that cause ripe rot [7,9[7][9][38][50],38,50], there is significant variation in the symptoms that manifest on other parts of the grapevine, such as flowers, leaves, and canes. Certain species predominantly affect berries and usually do not cause noticeable symptoms on most infected grape parts. These species include C. fructicola Prihast., L. Cai & K. D. Hyde [35[35][51],51], C. gloeosporioides s.s. [51], and C. tropicale E. I. Rojas, S. A. Rehner & Samuels [35], as well as C. fioriniae Marcelino & Gouli and C. nymphaeae (Pass.) Aa (which is a member of the CASC [12,51][12][51]). Conversely, some members of the CGSC can also cause a multipart rot of the grapevine apart from the berries alone, such as black spots, blight, and canker on other grape parts like flowers, leaves, and other vegetative tissues. Notable examples include C. aenigma [32], C. viniferum [8[8][32][39],32,39], and other C. gloeosporioides s.l. [7[7][52][53],52,53], which have yet to be conclusively identified through rigorous molecular analysis. Interestingly, although this has not been consistently observed, there are occasional reports of C. gloeosporioides s.s. causing localized leaf lesions [54], and C. viniferum causing necrotic lesions similar to the hypersensitive reaction on leaves [51]. C. siamense has been established as one of the causative pathogens of ripe rot in the table grapes variety V. vinifera ‘BRS Vitória’ in Brazil [36]. However, according to unpublished data, C. siamense (which is occasionally isolated from necrotic young grape berries), showed no pathogenicity on the berries of the hybrid variety V. labrusca × vinifera cv. Kyoho. There is a range of literature on C. siamense; some reports indicate leaf infections [32], while others describe it as a saprophyte on grapes [51,55][51][55]. These variations might be attributed to the intricate interplay between grape cultivars, the differences in virulence of the causal strain or CGSC, and even environmental factors [5,9,30,34][5][9][30][34]. Other species within the CGSC, such as C. conoides and C. temperatum, have also been suggested to be linked to grape ripe rot, though their pathogenicity on berries remains uncertain [4,12][4][12]. An intriguing exception within the naming convention of grape diseases related to Colletotrichum spp. is worth underscoring. In most plants, “anthracnose” often refers to diseases caused by Colletotrichum spp. [56,57,58][56][57][58]. However, in grapevine, “anthracnose” is specifically designated for a disease caused by Elsinoe ampelina (de Bary) Shear, which exhibits symptoms distinct from the classic ripe rot. These manifest as sunken necrotic lesions with grayish centers and brownish margins on berries, stems, and shoots, as well as small dead areas on leaves that lead to irregular holes [2,59][2][59]. Interestingly, certain Colletotrichum species have been reported to induce symptoms that are similar to the anthracnose caused by E. ampelina. Examples include C. gloeosporioides s.l. in India and the Philippines [60[60][61],61], along with species of other complexes such as C. acutatum s.l. and C. capsici s.l. in India [62,63][62][63], and C. fioriniae (CASC) in the U.S. [64]. The diversity of symptoms caused by Colletotrichum on grapevine highlights the critical necessity of precise identification in pursuing efficacious disease management, especially considering the different effects on the grape tissues across the Colletotrichum species. The berry-rot type of the grape rot disease caused by CGSC will particularly be further discussed in greater detail in the subsequent sections.

4. CGSC Life Cycle and Infection Factors

Gaining insights into the complex interactions between environmental factors, pathogens, and hosts is crucial for predicting the disease occurrences in grapevines. As the epidemiology and life cycle of the CGSC are explored, a deeper understanding of these intricate relationships will contribute to our overall knowledge of plant–pathogen interactions and their influence on grapevine health.

4.1. Pathogen

4.1.1. Lifestyles and Infection Processes

Colletotrichum species share similar, although not identical, lifestyles that are influenced by pathogen species, the disease resistance of the host tissue and its physiological maturity, as well as environmental conditions [65]. Nevertheless, the diversity of the symptoms observed on the grapevine organs other than on the berries also reflect the variety in their lifestyles within different parts of the grapevine. During berry infection, histopathological studies have generally shown that some C. gloeosporioides s.l. exhibit a hemibiotrophic lifestyle [66,67][66][67]. As conidia germinate on grape berry surfaces, appressoria form—which are positively correlated with grape rot disease severity—produce penetration pegs and enzymes, as well as breach the cuticle within a week after inoculation [66,67,68][66][67][68]. Fungal growth halts until veraison and then resumes inter- and intracellularly, ultimately leading to cellular collapse, necrosis, and ripe rot symptoms that develop as mature acervuli emerge [66]. Similarly, when C. viniferum was inoculated on pea-sized berries, the symptoms developed only after veraison [8], which also suggests a latent infection and the possibility of a hemibiotrophic lifestyle during berry infection. In regard to the infections on grapevine organs other than on berries, species such as C. fructicola-like and C. aenigma isolates do not induce symptoms. However, they do produce acervuli on blooms, suggesting a biotrophic lifestyle or endophytic behavior on asymptomatic flowers [12]. In contrast, C. viniferum causes severe necrosis on blooms, and undergoes significant secondary conidiation, indicating a primarily necrotrophic lifestyle [8].

4.1.2. Overwintering Structures and Primary Inoculum Sources

Several studies have demonstrated that CGSC members can overwinter in various grape tissues such as nodes, tendrils, pedicels, or peduncles, as well as debris, such as mummified berries and necrotic or desiccated leaves [8,69,70][8][69][70]. Additionally, sclerotia have been observed in some C. viniferum cultures [9], suggesting sclerotium as a possible overwintering structure in the field. Under favorable conditions for sporulation, water-dispersed conidia have the potential to be carried onto new tissues such as flowers, tendrils, leaves, or young berry clusters. Once there, the conidia germinate and either induce advanced symptoms or establish quiescent or latent infections [8,12,35,52,70,71][8][12][35][52][70][71] depending on the species and the interaction between the hosts. Furthermore, perithecia or ascospores, which are potentially spread by wind, have been observed in CGSC species such as C. viniferum and others [6,9,53][6][9][53]. Observations of the potential wind-mediated dispersal of CGSC members have also been reported [4]. Collectively, this evidence indicates that the causal CGSC members of ripe rot may employ both water and wind as vectors for dissemination, subject to environmental conditions.

4.1.3. Secondary Inoculum Sources and Infection Dynamics

Compared to primary inoculum, secondary inoculum are more closely correlated with disease severity for polycyclic pathogens such as Colletotrichum spp. [72,73][72][73]. As different species can cause varying levels of signs on the plant parts, the location and quantity of secondary inoculum may also vary. Colletotrichum spp. can undergo secondary conidiation on asymptomatic tissues; for instance, C. fructicola-like isolates can produce conidia on unblemished flowers [12]. Even more notably, C. viniferum have been observed producing conidia on necrotic flowers. When blooming inflorescences are infected with C. viniferum, the symptoms can involve necrosis on various parts, such as rachises, subrachises, and flowers, with the flower cap (calyptra) being the most susceptible (unpublished data). The infected deciduous calyptras, which carry abundant conidia, are very lightweight and can be blown in any direction, potentially leading to secondary infections. Although the infection pattern of individual CGSC members during the host bloom stage is yet to be comprehensively understood, observations indicate that flowers infected by CASC species (C. acutatum s.l.) result in an increase in disease incidence in the subsequent berry clusters [74,75][74][75]. In contrast, Cosseboom and Hu (2022) [4] suggest that infection at the bloom stage may not be as crucial as it is in the fruit stage.

4.2. Host: Susceptibility of Berries to CGSC Infection

Various studies have examined the susceptibility of grape berries to CGSC infection at different physiological stages. Daykin (1984) [69] found that berries are equally susceptible to C. gloeosporioides s.l. at all stages, while Fukaya (2001) [70] reported susceptibility until the stone-hardening stage. In contrast, Cosseboom and Hu (2022) [4] observed the ontogenic susceptibility of berries in natural infections by Colletotrichum spp. that consisted primarily of the CASC and a few CGSC members, with the stage after veraison being significantly susceptible. Nonetheless, the variability in berry susceptibility across the different studies can be attributed to several factors. These may encompass the particular species of Colletotrichum involved, the resistance levels of grape cultivars, and the complex interactions between grape cultivars and specific CGSC species [29].

4.3. Environmental Factors

The impact of environmental factors on grape berry infection by the artificial inoculation of C. gloeosporioides s.l. has shown that optimal infection conditions arise when the temperature is within the 25–30 °C range, and when there is a minimum wetness duration of 8 h [68]. A long-term vineyard monitoring spanning 12 years revealed that conidia from overwintered inoculum were released when three consecutive days exhibited temperatures above 15 °C, mean minimum temperatures that exceeded 10 °C, and a total precipitation surpassing 10 mm during that period [70]. Additionally, rainfall influences leaf wetness duration and strongly correlates with the dispersal of C. gloeosporioides s.l. conidia [69,70][69][70]. Ji et al. (2021) [71] developed a simulation model that considered the dynamic influence of weather on the epidemiology of the grape ripe rot caused by Colletotrichum spp. The model predicted disease occurrence by incorporating the effects of rainfall, temperature, and host susceptibility on fungal infection and sporulation processes. The accuracy of the prediction model was validated using field data, demonstrating its potential for supporting decision making in vineyard management practices and in improving the timing of fungicide applications. Cosseboom et al. (2022) [11] developed a comparable model, but with a focus on C. fioriniae, which is a CASC member. Nevertheless, it is important to highlight the distinctions between the CGSC and CASC species in terms of infection strategies, environmental conditions, and tissue preferences, as was discussed above. Therefore, despite the similarities in their general life cycles, studies focusing on the predominant CASC species need to be carefully adapted to understand the CGSC.

5. Changes in the Primary Causal Species

It is essential to recognize that dominant species can undergo shifts over time due to factors such as environmental conditions, host resistance, and fungicide application. Additionally, climate change and human activities potentially play influential roles, thus underscoring the importance of sustained research in this domain [76,77,78][76][77][78]. In India, climate change has been implicated in C. gloeosporioides s.l. replacing E. ampelina as the dominant pathogen causing anthracnose in grapevines [79]. The Colletotrichum species that causes ripe rot in grapes constitutes a diverse group of fungal pathogens. Given the complexity and diversity of their infection dynamics as mentioned above, it becomes imperative to understand the population dynamics of these species to devise effective strategies for maintaining the health of grapevines. Initially, in Taiwan, the CGSC species that caused no symptoms on leaves, likely C. fructicola, were postulated to be the prevalent pathogens for grape ripe rot [35]. However, a shift is evident in recent studies, where C. viniferum, a species within the CGSC that possesses different and stronger virulence toward berries and other grapevine parts, has emerged as the predominant pathogen [8,80][8][80].

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