Abstract
Phytophthora crown rot (PhCR) caused by Phytophthora cactorum is one of the most damaging soilborne diseases of strawberry in the United States and worldwide. Limitations on fumigants such as methyl bromide have led to deterioration in the control of P. cactorum in recent years. The development of resistant varieties is a critical component of the strategy for combatting this soilborne disease. Here, we review the biology of the pathogen, molecular mechanisms of infection, and management of PhCR in strawberry. Recent genomics advances in octoploid strawberry breeding have been able to gain a deeper insight into the genetic architecture of resistance to PhCR and identified the genetic resistance sources for the improvement of strawberry varieties against the pathogen. Quantitative trait loci (QTL) associated with PhCR resistance have been identified and introgressed for breeding of PhCR resistance in cultivated octoploid strawberry (F. × ananassa). Further characterizing candidate genes and mechanisms of resistance could facilitate incorporating the resistance genes into commercial varieties through genomics-assisted breeding, respectively. In this review, we address important recent advances and progress for genomics-assisted breeding for the resistance to PhCR and the potential use of CRISPR gene editing in cultivated strawberry.
Introduction
Strawberry is one of the important soft fruit crops popular for its color and taste. Besides its attractive color, strawberry has various health benefits such as high in vitamins, minerals, antioxidants, flavonoids, and phenolic acids (). The cultivated strawberry (Fragaria × ananassa) is an allo-octoploid (2n = 8x = 56) and interspecific hybrid originated from a cross between wild octoploid species F. chiloensis and F. virginiana (; ). In 2017, the United States produced 1.6 billion pounds (726 million kg) of strawberries, with a total value of approximately $3.5 billion (NASS, 2017). The yield and quality of strawberry fruit are affected by various environmental and biological factors. The common strawberry diseases in Florida include charcoal rot (Macrophomina phaseolina), Colletotrichum crown rot (Colletotrichum gloeosporioides), Botrytis fruit rot (Botrytis cinerea), Phytophthora crown rot (Phytophthora cactorum), anthracnose fruit rot (Colletotrichum acutatum), powdery mildew (Podosphaera apahanis), leather rot (P. cactorum and P. nicotianae), Phomopsis leaf blight and soft rot (Phomopsis obscurans), stem end rot and leaf blotch (Gnomonia comari), and angular leaf spot (Xanthomonas fragariae) (Oliveira and Peres, 2020).
Among various diseases, economic losses due to root and crown rots are estimated about $150 million per year in the United States (Samtani et al., 2019). In the Florida industry itself, it is estimated that yield loss due to soilborne diseases costs $15 million in revenue each year, despite annual pre-plant soil fumigation (personal communication with Florida Strawberry Growers Association). Phytophthora crown rot (PhCR) disease caused by P. cactorum is one of the most important soilborne diseases of strawberry in the United States and worldwide, causing up to 40% production losses (Stensvand et al., 1999). This pathogen was first reported in Germany in 1952 () and has been problematic in strawberry production worldwide (Schafleitner et al., 2013).
Limitations on fumigants have imposed challenges for the control of P. cactorum in recent years. Commercial cultivars vary widely in their genetic resistance to this pathogen, with the most resistant varieties providing high levels of disease control (Mangandi et al., 2017). Thus, the development of resistant cultivars will be a critical component of the strategy for managing this disease in an era of limited fumigants and increases in demand for organic strawberries. Also, soil fumigation before planting is often ineffective in controlling this disease in fruit production fields because the main inoculum source is infected nursery stock (; ). Although various practices together with chemical pesticides are used to manage PhCR, understanding the mechanism of disease resistance and developing disease-resistant cultivars is the best strategy to protect against the pathogen.
Several breeding efforts have been made in the past to identify the genetic resource of resistance for breeding in both diploid and octoploid strawberries (; Shaw et al., 2006; Shaw et al., 2008; ). The resistance locus Resistance to Phytophthora cactorum 1 (RPc-1) has been identified in F. vesca (). In the octoploid cultivated strawberry, a major resistance locus, FaRPc2, located in a linkage group 7D confers resistance against P. cactorum (Mangandi et al., 2017). Other quantitative trait loci (QTL), FaRPc6C, FaRPc6D, and FaRPc7D, were also identified in a biparental mapping population for P. cactorum resistance in cultivated strawberry (Nellist et al., 2019). FaRPc2 and FaRPc7D are located in the same genomic region, indicating the same resistance QTL. Pathogen populations can be constitutively diversified in response to resistance genes in plants and high levels of diversity and population structure are observed in the potato late blight pathogen, P. infestans (Wang et al., 2017). It would be important to understand the population genetic structure of pathogens for crafting durable resistance and addressing the potential breakdown of resistance genes in field conditions. Currently, there is no information available about the pathogenic diversity of P. cactorum in U.S. strawberry fruiting fields and plant nurseries. It is not uncommon to observe pathotypes of other Phytophthora species in soybean and potato, as these pathogens have rapidly adapted to overcome resistance genes (Witek et al., 2016; Rojas et al., 2017). In addition, a recent study reported that another Phytophthora species, P. nicotianae, which is closely related to P. cactorum, can cause crown rot of strawberry in the United States (Marin et al., 2018). Unfortunately, little is known about how P. nicotianae compares to P. cactorum with respect to host resistance, especially for FaRPc2, which is the major resistance source for strawberry varieties in the United States. The spatial and temporal deployment of resistance genes of FaRPc2 combined with knowledge of pathogen populations would be a major factor determining broad-spectrum resistance to PhCR in cultivated strawberry.
This review addresses the current knowledge of P. cactorum causing crown rot disease and its management, and recent genomic approaches for the breeding of PhCR resistance in cultivated strawberry.
The genus Phytophthora and P. cactorum causing Phytophthora crown rot disease in strawberry
The genus Phytophthora became widely known among plant pathologists after the late blight disease of potato, caused by Phytophthora infestans, in the United States, in 1843, and in Europe, in 1845 (; Peterson et al., 1992). The pathogen destroyed Ireland’s potato fields during 1845–1846, leading the country to mass starvation with sociological and economic impacts (Large, 1940). The genus was first described by de Bary, in 1876 (). Within this genus, several species are described, some with a narrow host range while others are pathogenic to more than 900 plant species, such as P. infestans and P. cinnamomi, respectively (Zentmyer, 1980). Moreover, adaptability, such as hybridization and effective dispersal, have enabled Phytophthora species to shift hosts, colonize new niches, and become more aggressive and invasive pathogens (; ; Man in ‘t Veld et al., 2012; Husson et al., 2015).
Taxonomically, the species P. cactorum is within the kingdom Stramenopila, phylum Heterokontaphyta, class Peronosporomycetes, order Peronosporales, and family Peronosporaceae. This hemibiotrophic oomycete pathogen has been reported for the first time from rotting cacti (Cereus giganteus and Melocactus nigrotomentosus) by Lebert and Cohn (1870) in Czechoslovakia. Several synonyms are listed by , but P. cactorum is the valid name nowadays. Although it occurs worldwide, it is mostly found in temperate regions causing root and collar rots, fruit rots, cankers, leaf blight, wilts, and seedling blights in various hosts (). This pathogen can cause disease in more than 200 plant species from 150 different genera and 60 families (Tucker, 1933; Nienhaus, 1960). In strawberry, P. cactorum was first reported to cause leather rot on fruit (Rose, 1924), then crown rot, in 1952 (). Since then, crown rot of strawberry caused by this Phytophthora species has been detected in most of the United States, Europe, and parts of Asia and Africa.
P. cactorum is a homothallic species producing oospores on several natural media (). Oogonia features are smooth-walled and hyaline (19–38 µm diameter); antheridia are paragynous and often attached close to the oogonial stalk; oospores could be plerotic or aplerotic within a range of 20–26 µm in diameter. Sporangia are papillate, normally borne terminally, with shape ranging from ellipsoidal to spherical (31.4 ± 4.8 × 26.4 ± 4.0 µm) (Oudemans and Coffey, 1991; ). Sporangiophores are often simple or in a close or lax sympodium with clustered sporangia (; ). Chlamydospores are not very often produced, but when present, they are terminal or intercalary and globose (17–55 µm in diameter). Colonies have no distinct pattern in V8 agar, potato dextrose agar, and malt extract agar with cardinal temperatures of 4°C for minimum, 24°C for optimum, and 30°C for maximum growth ().
P. cactorum shares the Clade 1a of the Phytophthora phylogenetic tree based on the internal transcribed spacer (ITS) region with P. idaei, P. pseudotsugae, and P. hedraiandra (). Its distinguishable features from the other species are the production of caducous sporangia with short pedicels (less than 40 mm) and paragynous antheridia (). Besides morphology, BLASTs of the ITS and cytochrome c oxidase subunit 1 (COI) regions are often used for Phytophthora species identification (Robideau et al., 2011). However, a method for routine and rapid detection of P. cactorum was created based on high-resolution melting (HRM) assay, which facilitates correct diagnosis, the study of their host ranges and distributions, and accelerates management decisions (Ratti et al., 2019).
Morphology of sporangia and oogonia can slightly vary among P. cactorum isolates from different hosts, but due to subtle variations, these characteristics are not enough for isolate differentiation (). However, some molecular markers can distinguish among isolates from different plant species (; ; Lilja et al., 1998). Variations can also be observed among isolates from the same host infecting different tissues, such as isolates infecting strawberry crown and fruit, causing crown rot and leather rot, respectively. For a long time, it has been believed that crown rot could only be caused by strains isolated from strawberry crowns or from soil, whereas isolates from other hosts and strawberry fruit could produce leather rot (Seemüller and Schmidle, 1979; ; ). Although crown rot is likely caused by a genetically distinct pathotype of P. cactorum, isolates have the ability to cause leather rot on strawberry; however, not all isolates from leather rot have the ability to cause crown rot (; Nellist et al., 2021). Additionally, genetic separation among isolates of P. cactorum in North America and Europe was not obtained with UPGMA analysis; however, host specificity among the strains was observed. Contrastingly, AFLP markers showed that leather rot isolates were different from crown rot isolates during the analysis of 44 isolates of P. cactorum from strawberry and other hosts (). Besides P. cactorum, other species can also be associated with causing crown-rot-like symptoms. Phytophthora fragariae causes red stele (red coloration in the core of the root), which can be significant in some strawberry-growing regions leading to severe stunting and mortality. Other species of Phytophthora have also been occasionally reported in strawberry, such as P. citricola, P. citrophthora, P. eryptogea, P. bishii (= bisheria), P. megasperma, P. fragariaefolia, and P. nicotianae (Jeffers and Scott 1953; Meszka and Michalecka 2016; Marin et al., 2018; ).
Biology of Phytophthora cactorum on strawberry plants
Disease and symptoms
PhCR of strawberry can be caused by several Phytophthora species; however, P. cactorum is the most important. Early symptoms are characterized by young leaves turning bluish-green, which eventually begin to wilt. Due to disease development and crown collapse, the whole plant wilts and dies within days (Peres and Baggio, 2019). When the diseased plant is removed from the ground, the crown likely breaks at the upper end. Dark reddish-brown discoloration of crowns starting at the upper or bottom part and disintegration of the vascular tissue are characteristic symptoms of this disease (Figure 1), which could be confused with symptoms caused by other crown rot pathogens, such as C. gloeosporioides and M. phaseolina. Depending on the environmental factors, the number of crowns within the plant, and cultivar tolerance, the rotting process of the crown may stop leading to recovery or stunting of the plant (Maas, 1998).
Figure 1
Pathogen biology, epidemiology, and disease cycle
Pathogen infection and disease development require specific factors and, if not fulfilled, infections may remain latent, such as in cold-stored plants. Warm weather and abundant wetness trigger disease occurrence and development (Maas, 1998). In strawberry annual production systems in open fields that adopt overhead irrigation after transplanting to promote plant establishment, these conditions are common, leading to outbreaks in the early season of diseases caused by oomycetes (Marin et al., 2019; ). Strawberries are more susceptible at transplanting, and 45 to 60 days later, which correspond to periods when the plant is metabolically more active due to rapid juvenile growth, root development, and fruit production (Marin et al., 2022a). Constant availability of new root growth is a likely cause of the rapid development of damaging Phytophthora populations under favorable conditions. Although cultivar resistance is genetically determined, digging immature plants from the nursery could lead to outbreaks in fruit production fields. Moreover, plants under stress are more prone to disease development, such as frigo plants transplanted during warm weather (Lederer and Seemuller, 1992).
The disease cycle may slightly change depending on the strawberry production system (Figure 2). For the perennial production system and nursery fields, due to the constant presence of strawberry plants, the source of inoculum could be oospores that are produced from sexual reproduction between antheridium and oogonium and survived in the soil or plant debris (Srivastava et al., 2020). This survival structure, under conducive conditions, germinates and produces sporangium that contains zoospores. Either the germinated sporangium or the flagellated zoospores can infect the plants, usually through wounds during transplanting. Zoospores move in the water, discard flagella, and synthesize a cell wall, forming a cyst. The cyst germinates and enters host tissue through natural openings like stomata or penetration of host epidermal cells that occurs with the help of an appressorium-like swollen tube (Hohl and Stössel, 1976). Specifically for nursery production, cold-stored plant material (frigo plants) could also serve as the major source of inoculum (Pettitt and Pegg, 1994). The expression of symptoms is linked to the time of planting, since during winter, the pathogen reduces its activity due to low temperatures, delaying disease progress (Maas, 1998). For annual strawberry production, where plants are usually cultivated during the winter, the pathogen might not survive between production seasons, during summer. In Florida, through nurseries monitoring and studies aiming to access the Phytophthora survival over seasons, the major source of inoculum is likely transplants harboring quiescent infection from nurseries (); however, this scenario could be different for strawberry growing regions lacking such information. The strawberry propagation system in nursery fields varies, but it is common that at least the third and fourth generations of transplants are multiplied in open fields, being subjected to pathogen infection (Rahman et al., 2015). A similar situation could happen at the nursery level with the exchange of plant stock materials within and among nurseries. After introduction of the pathogen in a field, under wet and favorable conditions, zoospores are produced by infected plants and can disseminate at short distances through free water present in poorly drained soil and penetrate strawberry plants. However, these secondary infections are more likely to occur at the nursery level or in perennial production systems, where the density of plants is higher and plants are maintained in the fields for longer periods, resulting in multiple disease cycles within one crop cycle, characterizing a polycyclic disease. Conversely, in annual production systems, where secondary infections are rare during the same crop cycle, the disease has a monocyclic pattern of development.
Figure 2
Disease management—cultural control
PhCR is usually managed with a combination of chemical and non-chemical methods. Cultural control methods can vary depending on the strawberry region and production system adopted. Studies carried out in Florida, where the annual production system is adopted, show that the pathogen inoculum likely does not survive in the soil and asymptomatic nursery transplants harboring latent infections are considered the major source of inoculum (). However, the inoculum survival could greatly vary according to weather and soil type among different strawberry growing regions; therefore, more studies aiming to monitor the inoculum survival over time in other areas are needed, such as the one carried out by . Foremost, the acquisition of free and clean plant stock is detrimental to avoid the introduction of the pathogen and the start of an epidemic. In perennial production systems, where the pathogen can survive in the soil and plant debris, practices that aim to eliminate or reduce the inoculum present in the soil are usually adopted. Among these methods, soil fumigation and soil solarization have been reported to be effective in controlling Phytophthora species. Solarization is carried out after the beds are formed and can be effective if weather conditions are ideal (30–45 days of hot weather that promotes soil temperatures of at least 50°C). Also, steam disinfestation could be used as an alternative to chemical fumigation, since raising the soil temperature to 70°C for 30 min to a depth of 0 to 25 cm effectively reduced soilborne diseases ().
Regardless of the production system, PhCR incidence is usually lower in sites with appropriate soil drainage. Improved soil drainage is usually achieved with properly prepared and tilled soil, preventing the formation of soil layers that are impervious to water. The pathogen could also be introduced in a disease-free area from infested areas through contaminated irrigation water. Therefore, the adoption of appropriate irrigation practices, such as reducing overhead irrigation to avoid free water availability and monitoring water from reservoirs for pathogen occurrence, could avoid the introduction and minimize the dissemination of the pathogen in a field. The adoption of plastic-mulched, raised beds also contributes to disease management. Besides permitting the use of drip irrigation systems, in which low amounts of water are provided to the plants, it improves soil drainage and allows the application of soil fumigants, which can help with inoculum reduction in soils infested with Phytophthora species.
To manage diseases in the plant stock materials at the nursery level, thermotherapy of asymptomatic nursery transplants infected with P. cactorum could be a good alternative to manage pathogen populations in plant stock. Studies have shown that exposing transplants to aerated steam in a closed chamber at 37°C for 1 h, followed by 44°C for 4 h, was effective in reducing P. cactorum, including mefenoxam-resistant populations and disease incidence in production fields (). The other chemical alternative would be the use of biological products; however, their efficacy may vary across different seasons if environmental conditions are not always conducive to the biological agent (Hautsalo et al., 2016). Some products containing Streptomyces spp., Bacillus subtilis strain AFS032321, and Pseudomonas chlororaphis strain AFS009 were tested at field conditions in Florida and had a positive effect on reducing PhCR (Mertely et al., 2020; ). However, more studies are needed to really access their efficacy across multiple seasons in Florida and different strawberry growing regions.
The adoption of tolerant or less-susceptible cultivars is a desirable strategy and a sustainable method in managing PhCR. Among some of the FL and CA cultivars, ‘Sweet Charlie’, “Florida Radiance’, ‘Florida 127’ Sensation™, and ‘Florida Brilliance’ are susceptible, whereas ‘Strawberry Festival’, ‘Florida Elyana’, ‘Florida Beauty’, ‘Fronteras’, ‘Merced’, ‘Albion’, ‘San Andreas’, and ‘Portola’ are considered tolerant ; Marin et al., 2022a). Unfortunately, most cultivars are bred and selected based on fruit yield and quality and not on tolerance to PhCR. Therefore, it falls on breeding programs for the development and deployment of new cultivars with pathogen resistance, fruit quality, and competitive yield.
Disease management—chemical control
In areas where the pathogen may survive in the soil, soil fumigation can provide adequate control of the disease. Nursery and fruit production growers have always relied on soil fumigation using methyl bromide due to its high effectiveness in controlling soilborne pathogens (Santos et al., 2006). However, its phase out in 2013 in the United States and being banned in the EU from 2010 led producers to transition to alternative broad-spectrum fumigants, such as chloropicrin, 1,3-dichloropropene, metam sodium, dazomet, allyl-isothiocyanates, methyl iodide, dimethyl disulfide, and ethanedinitrile, which are usually not as effective (; Holmes et al., 2020). Limitation of the product movement throughout the soil profile due to its chemical features may jeopardize the reduction of pathogen population in the soil. Regardless of the production system, fungicide applications during transplanting and fruit production are still the predominant control method and, basically, only metalaxyl or mefenoxam and potassium phosphite products are available and registered for strawberry production in the United States (Peres and Baggio, 2019). However, due to the emergence of mefenoxam-resistant isolates and the failure of phosphite products in controlling P. nicotianae, management of PhCR has become even more challenging (Marin and Peres, 2021; Marin et al., 2021). Moreover, even resistance to quinone outside inhibitor fungicides has been reported in P. cactorum and P. nicotianae in Florida (Marin et al., 2022b). Thus, there is a demand for further research to find more effective alternative broad-spectrum fumigants and/or more efficient application methods, fungicides with new modes of action, and alternative biorational products. To improve the management options, alternative oomyticides were investigated and potential products were found; however, they are still not registered for strawberry (Marin and Peres, 2021). Moreover, disease management must be based on integrating the adoption of tolerant cultivars, cultural practices, and chemical applications to minimize the limitations of each control method.
Molecular mechanisms for the pathogen infection in strawberry
Various fungal pathogens use plant cell-wall degrading enzymes like CAZymes and mechanical force to break those barriers to infect and extract nutrients from the host cell. A total of 696 transcripts encoding CAZymes targeting cellulose, hemi-cellulose, and pectin were identified in the genome of P. cactorum 10300 (). Plant cell wall degrading enzymes, protease inhibitors, and phytotoxins of the PcF Toxin family are the effectors deployed by Phytophthora spp. during the infection of the host (). The delivery of various effector proteins (apoplastic or cytoplasmic) into the host tissue by a virulent pathogen targets plant immune system-related proteins () and helps them to defeat plant immunity and initiate infection (). These effectors are secreted into the apoplast or host cells with the help of haustoria (Petre and Kamoun, 2014). In most of the Phytophthora species, a conserved RXLR motif at the N terminus is contained in one of the important classes of cytoplasmic effectors (Jiang et al., 2008). Various avirulence proteins (RXLR cytoplasmic effectors) like PiAvr3a, PiAvr2, PiAvr4, and PiAvrB1b1 has been localized to haustoria showing it as a site of secretion and delivery into host cells (; van Poppel, 2009; ). The presence of infection-induced haustorium membrane protein 1 (PiHmp1) is important for infection in potato by P. infestans (). The importance of this protein for infection is highlighted with transient silencing of PiHmp1 that prevented infection to the host tissue.
Transcriptomic profiling of three different life cycle stages (mycelia, zoospores, and germinating cysts with germ tubes) of P. cactorum revealed the induction of numerous RXLR and Nep1-like proteins (NLPs) and the downregulation of the majority of Crinklers (CRNs) genes in germinating cysts with germ tube stage (). Since cyst with the germ tube stage is an important pre-infection stage, the upregulated genes play a major role during the infection to host tissue. Moreover, gene expression patterns before and after the infection by P. cactorum identified various RXLR effector genes (). Transcriptomic analysis of P. cactorum revealed a gene encoding the small cysteine-rich secretory protein SCR96 to be a virulence factor and important for oxidative stress tolerance (). The comparison of transcriptomes of two P. cactorum isolates Pc407 (high virulence) and Pc440 (low virulence) obtained from Fragaria vesca revealed the high expression of a gene encoding a GAF sensor protein in the high virulence isolate Pc407 that is potentially involved in membrane trafficking processes (Taljoma et al., 2019). Lipid catabolism and elicitins were more highly expressed in Pc407 than in Pc440 at 48 h post-inoculation. The members of the glycosyl hydrolase family 1 involved in the metabolism of glycosylated secondary metabolites were expressed more in Pc407 than in Pc440. In addition, the more virulent isolate Pc407 depends on a smaller set of key RXLR effectors while infecting the host tissue whereas the less virulent isolate Pc440 relies on more RXLR effectors. We propose that P. cactorum infection in strawberry would involve a cascade of enzymes and effectors to infect plants similar to the infection mechanism used by other Phytophthora species.
Genome sequencing of P. cactorum and its application to control Phytophthora crown rot
The exploitation of DNA sequencing helped in learning more about the genetics of Phytophthora, species differentiation, phylogeny construction, and grouping into clades (). The availability of isolate sequences would help to identify similarities and differences in addition to showing if any gene or DNA region is identical (or nearly identical), in which case the isolates belong to the same species. P. cactorum infects a wide range of plants including ornamentals, trees, and fruit crops. The whole genome sequencing of P. cactorum from Panax species revealed its genome size to be 121.5 Mb using third-generation single-molecule real-time (SMRT) sequencing technology (Yang et al., 2018). The genome is highly heterozygous and is the second largest genome within the Phytophthora genus. On comparing the genome of P. cactorum with other Phytophthora spp., it was revealed that P. parasitica, P. infestans, and P. capsici had the closest relationships (highly syntenic). The extensive expansion of genes encoding detoxification enzymes and carbohydrate-active enzymes (CAZymes) showed comparative analyses of Phytophthora genomes. Also, due to the wide host range, P. cactorum had higher utilization or detoxification ability against ginsenosides (a group of defense compounds synthesized by Panax species) compared to P. sojae. A total of 901 and 282 genes were predicted to putatively encode CAZY enzymes in P. cactorum from Panax and strawberry, respectively (). Also, tolerance to fungicides in P. cactorum involved many proteins in the detoxification metabolic pathway, revealed by proteomic analysis (Mei et al., 2014). The identification of peroxidase (POD), glutathione S-transferases (GST), cytochrome P450 (CYPs), methyltransferase (MTR), dehydrogenase, ATP-binding cassette (ABC) transporter families, and major facilitator superfamily (MFS) in P. cactorum genome supports the ability of the pathogen to detoxify secreted ginsenosides (Yang et al., 2018).
Utilizing de novo prediction and homology-based comparison, the genome of P. cactorum was found to have 56.7 Mb repetitive elements, which constitutes 46.7% of the assembled genome (Yang et al., 2018). Of the 46.7% repetitive elements in the genome, 45.3% include transposable elements (TEs), 20.3% of which include long terminal repeats (LTR). The majority of unique genes in P. cactorum were related to defense response, the cell cycle, interaction between organisms, regulation of the cell cycle, TOP signaling pathway, and peptidyl-amino acid modification. The genome sequence of P. cactorum isolate 10300 isolated from infected strawberry tissue generated a 59.3-Mb genome assembly with a de novo assembly using ABySS (). The genome size of P. cactorum from strawberry is smaller compared to the genome of P. cactorum from Panax species (121.5 Mb). Also, the percentage of repetitive elements is 18% in the P. cactorum genome from strawberry versus 46.7% in the genome from Panax. A total of 23,884 genes encoding 24,189 proteins were predicted from its genome, and the number of genes that encoded putatively secreted proteins was 2,234. Although the numbers of genes predicted might be variable within Phytophthora species, the greatest number of complete single copy core eukaryotic genes (CEGs) was obtained in P. cactorum gene models, indicating a good representation of gene space within gene models ().
The predicted genes revealed a plethora of genes encoding putative secreted effectors containing about 200 RxLR domain-containing effectors, 77 CRNs, and apoplastic effectors such as phytotoxins (PcF proteins) and necrosis inducing proteins that play a significant role in infecting the host tissue. Genome sequencing and comparative analysis of 18 isolates of P. cactorum revealed evidence for host specialization (). Isolates causing PhCR in strawberry are globally similar whereas greater diversity was observed for apple-infecting isolates. Discrete lineages and non-recombining clades were observed within P. cactorum for specialized strawberry PhCR and apple-specific isolates. Additionally, gain and loss of effector complements were observed in P. cactorum phylogeny presenting determinants of host boundaries. Although the genome sequencing and comparative analysis from different research highlight the role of RxLR effectors, CRNs, and apoplastic effectors, not much has been done to characterize their individual role in infecting strawberry. Additionally, understanding the host specificity of these effectors would allow us to target them for resistance breeding in strawberry to PhCR.
In the future, further genome sequencing of P. cactorum isolates and Phytophthora spp. would allow for a better understanding of the molecular mechanism of infection via comparative genomic analysis. It is crucial to identify and understand the effectors involved during infection to understand the molecular disease mechanism. Also, the durability and functionality of the disease resistance depend on the effector protein secreted by plant pathogens, and these isolate-specific effectors could be targeted for resistance breeding in strawberry. Furthermore, the availability of genome sequences for different isolates of P. cactorum would help in early detection and surveillance for a new isolate if they evolve in the future and to keep track of different isolates infecting strawberry. The comparative analysis of all the isolates of P. cactorum infecting strawberry would additionally provide information about conserved regions across all the isolates. This conserved regions across isolates might serve as the target region in the pathogen genome for resistance breeding against P. cactorum.
QTL discovery for the resistance to Phytophthora crown rot in strawberry
The majority of cultivars grown worldwide are susceptible to P. cactorum, although high level of resistance was observed in a few cultivated strawberries and numerous diploid strawberry accessions (Parikka, 2003; ). The diploid wild strawberry F. vesca ‘Hawaill 4’ genotype showed resistance against P. cactorum. A major locus, RPc-1 (Resistance to P. cactorum 1), identified from F. vesca explained 74.4% of the phenotypic variation for resistance to PhCR (; Toljamo et al., 2016). In addition to the diploid strawberry, different sources of resistance against P. cactorum are available in the octoploid strawberry (; Shaw et al., 2006; Shaw et al., 2008; Mangandi et al., 2017; Nellist et al., 2019). The testing of 26 cultivars and five selections for resistance to P. cactorum crown rot revealed that the genetic background greatly affects the degree of resistance and susceptibility to P. cactorum (). In another study, 186 genotypes from the University of California strawberry breeding program were evaluated for the resistance to P. cactorum and identified that the phenotypic variation of 60.6% for the PhCR resistance was due to the different genetic backgrounds among the genotypes (Shaw et al., 2006). The maximum resistance was observed for ‘Albion’, ‘Aromas’, and ‘Camino Real’, moderate resistance for ‘Camarosa’, and minimum resistance for ‘Diamante’ and ‘Ventana’ (Shaw et al., 2006). Conventional and biotechnological approaches could be used to transfer the source of resistance to susceptible cultivars.
In the strawberry breeding program of the University of Florida, a major locus conferring resistance to PhCR referring to FaRPc2 was identified using a pedigree-based analysis in complex, multiparental population sets (Mangandi et al., 2017). The resistance locus FaRPc2 was mapped to linkage group 7D and accounts for most of the genetic variation existing in the breeding population tested for the PhCR resistance. Within the FaRPc2 locus, it was found that two major haplotypes H2 (FaRPc2-H2) and H3 (FaRPc2-H3) are highly associated with resistance against P. cactorum. The two resistant haplotypes may be originated from different resistance sources, and it is possible that two distinct functional resistance alleles are present at FaRPc2. The FaRPc2-H3 genotype is more prevalent in commercial strawberry varieties in the United States, while FaRPc2-H2 seems to be more frequently present in European accessions (Noh et al., 2018). However, very little is known about molecular mechanisms of resistance and candidate genes in the FaRPc2 region. To achieve the long-term goal of achieving durable resistance against P. cactorum, it would be important to combine multiple resistance genes and/or alleles. Additionally, three QTLs (FaRPc6C, FaRPc6D, and FaRPc7D) were reported in European germplasm on chromosomes 6-2, 6-4, and 7-3 using biparental population (‘Emily’ × ‘Fenella’) inoculated in a greenhouse (Nellist et al., 2019). Three QTLs explained about 37% of the phenotypic variation (Nellist et al., 2019). The significant SNP markers for FaRPc7D were located within the same QTL region of FaRPc2. Biparental mapping population could detect locus-determining small genetic variability because it includes less genetic and allelic diversity from fewer parents. However, the use of multi-parental populations enabled the exploration of allelic diversity and increased the accuracy of QTL detection (Mangandi et al., 2017). Thus, QTLs identified using a multifamily population would be effective in diverse genetic backgrounds, whereas QTLs identified using biparental population might be less effective for wide genetic backgrounds.
Genomics-assisted breeding approaches for the resistance against P. cactorum
The application of genomics in strawberry breeding has lagged compared to other major crops because of its highly heterozygous allo-octoploid genome, and limited genomic resources in the past. However, the recent availability of reference genome of octoploid strawberry from 'Camarosa', SNP genotyping array (FanaSNP), and high-throughput DNA tests enabled the use of genomic approaches in strawberry breeding (; ; Whitaker et al., 2020; Oh et al., 2020; Liu et al., 2021). In addition, the recent haplotype-phased genomes from University of California variety 'Royal Royce' and University of Florida elite breeding line 'FL15.89-25' shed light on advanced genomics research in strawberry (; ). Several disease resistance traits are controlled by major loci such as FaRPc2, FaRCa1, and FaRCg1 (Mangandi et al., 2017; Salinas et al., 2019; ). In some cases, complex traits may not be controlled by a few loci, and the application of genome-wide prediction would be an alternative strategy for improving traits of interest (Whitaker et al., 2020; Tapia et al., 2022). Genome-wide prediction in strawberry had been used in the past for parent selection of positive yield and quality traits (Petrasch et al., 2022). This approach could be useful for predicting breeding values without phenotypic information (Whitaker et al., 2020).
The development of genetically resistant varieties against P. cactorum is the most reliable and long-lasting method to protect strawberry plants from the pathogen. The screening and identification of a durable source of resistance are essential to transfer the source into a susceptible variety. The classical breeding for resistance involved the transfer of R genes from one germplasm to another. Breeding efforts for P. cactorum resistance started in 1992, and mostly focused on testing methods for susceptibility in mature plants (Simpson et al., 1994). Genomic tools have been used to develop molecular markers tightly associated with candidate R genes in the selection of parents and predicting inheritance pattern in progenies for early selection, thus reducing the costs associated with field trials (; Peace, 2017). The development of the first 90K Axiom single nucleotide polymorphism (SNP) array enabled the identification of QTLs associated with the trait of interest to develop molecular markers (). A compendium of strawberry DNA tests was created and subsequently available to assist the breeders with the molecular markers available for various traits in strawberry (Oh et al., 2020). These DNA tests would help breeders to exploit the genetic resources available in their breeding program to breed better cultivars.
Rapid DNA extraction and high-resolution melting analysis were used for selection at the FaRPc2 loci conferring Phytophthora crown and root rot resistance in the strawberry breeding program at the University of Florida in 2015 (Lee et al., 2016). In addition, the development of high-throughput molecular markers and fine-mapping of FaRPc2 has been described in the octoploid strawberry (Noh et al., 2018). The high-resolution SNP molecular markers were developed for H2 and H3 haplotypes responsible for resistance to P. cactorum on strawberry. A total of seven markers for H2 (FaRPc2-H2) and four for H3 (FaRPc2-H3) resistance haplotype were tested for the University of Florida strawberry breeding population and other varieties from different breeding programs, respectively (Noh et al., 2018). All the markers were successfully utilized to breed new resistant varieties via marker-assisted selection.
Recently, the availability of reference genome and sequencing technologies helped to identify R genes associated with disease resistance in strawberry (; ; Shirasawa et al., 2021). The comparison of R genes present in cultivated strawberry with their diploid ancestors helped to understand their presence and retention during the transition from diploid to octoploid, and expression pattern (). The diploid ancestral relatives of the modern cultivated strawberry could possess genetic resources for disease resistance that could be introgressed to susceptible varieties.
Candidate genes and molecular mechanisms for the resistance against P. cactorum in strawberry
The R gene-related transcripts including receptor-like kinases, nucleotide-binding site leucine-rich repeat (NBS-LRR), and toll/interleukin-1 receptor domain-containing proteins were highly upregulated in the resistant genotype of F. vesca compared to the susceptible genotypes (). A PCR-based approach (NBS profiling) identified 23 distinct resistant gene analog fragments of NBS-LRR from a resistant genotype of F. vesca (). One of the RGAs, RGA109, was characterized as a putative NBS-LRR R protein. RPc-1 locus (resistant to P. cactorum) included one NB-LRR protein that was upregulated in resistant genotypes after the pathogen infection. Similarly, potential resistant genes were also identified in RPc-1 locus from root transcriptomic analysis of F. vesca (Toljamo et al., 2016).
Transcriptomic analysis of F. vesca ‘Hawaill 4’ roots infected with P. cactorum revealed potential candidate genes within the QTL region, RPc1, responsible for defense (; Toljamo et al., 2016). They identified 69 defense-related genes within RPc1; 7 were significantly downregulated, and 19 were upregulated in response to the P. cactorum inoculation. Several genes such as NBS-LRR, L-type-lectin-RKLs, and receptor-like protein (RLP) with a leucine-rich-repeat were highly expressed in inoculated plants. The L-type-lectin-RKLs are involved in Phytophthora resistance, while LRR-RLPs are associated with various disease resistance in plants (; Zipfel, 2014; Wang et al., 2015). A phenylalanine ammonia-lyase (PAL) encoding gene in RPc1 was upregulated after inoculation of P. cactorum. The PAL-dependent phenylpropanoid pathway is responsible for salicylic acid synthesis, which is an important hormone signaling pathway associated with fungal pathogen defense responses (Yuan et al., 2009). In addition, WRKY transcription factors located in RPc1 were significantly upregulated in response to P. cactorum inoculation. The transcriptomic analysis of F. vesca roots after inoculation with P. cactorum provides the possible molecular mechanisms for resistance associated with the pathogen in strawberry. All these RNA-seq transcriptome studies were carried out in diploid F. vesca, but none of the gene expression data in response to P. cactorum have been reported in the octoploid strawberry.
A number of candidate genes had been identified in plants for Phytophthora resistance; however, only limited work has been achieved in the octoploid cultivated strawberry. Analysis of transcriptome data was conducted for the resistance to C. gloeosporioides in octoploid strawberry (Wang et al., 2017;). identified several candidate genes for the resistance to Colletotrichum crown rot and developed functional markers linked to the major locus FaRCg1 conferring resistance against C. gloeosporioides. It is important to identify candidate genes and incorporate them into elite breeding materials for developing new resistant cultivars. Expression QTL (eQTL) analysis could also effectively discover gene associations with target traits of interests in strawberry (). This genomics approach successfully characterized important genes associated with fruit flavors and pathways.
Molecular mechanisms of defense against P. cactorum have not been understood in strawberry, although the defense mechanism of various horticulturally important plants against Phytophthora spp. is available. The defense system can be categorized as preformed and induced depending on how they respond to the attacking pathogen (Jones and Dangl, 2006). The preformed defense system responds to a different class of pathogens in a similar way. It includes cell wall, waxy epidermal layer, bark, and cuticle that act as the first line of defense used by plants against the pathogens. The induced defense system responds to the virulence factors or elicitors of the pathogen directly or effecting host targets to defend (Van Loon et al., 2006). The first line of defense in strawberry could include cuticle, cell wall, trichomes, and leaf veins against various pathogens such as B. cinerea, C. acutatum, Tetranychus utricae, and Xantomonas fragariae, respectively (; ; ; Steinite and Levinsh, 2003; Kennedy and King, 1962). Biochemical barriers present in various parts of strawberries acts as a defense against various pathogens. The secondary metabolites including glucosinolates, sulfur compounds, phenolics, and saponins form a biological barrier acting at early stage of infection (Kliebenstein, 2004). Salicyclic acid, lignin, and chlorogenic acid are products of the phenylpropanoid pathway and serve as barriers for pathogens in strawberry. A biochemical compound similar to phytoalexin acts to make strawberries resistant to P. fragariae (Mussell and Staples, 1971), whereas the presence of antifungal compounds in the strawberry leaves makes it resistant to Colletotrichum fragariae. The preformed compound had antifungal activity 15 times more in the moderately resistant cultivar 'Sweet Charlie' than in the susceptible cultivar ‘Chandler’ (Terry, 2002).
Pattern recognition receptors (PRRs) in the plant cell membrane expose their pathogen/microbe/damage-associated molecular pattern (PAMP/MAMP/DAMP) recognition domains into the apoplast that recognizes conserved oomycete PAMPs and trigger PAMP-triggered immunity (PTI) (). The recognition of pathogen’s effectors entering the host cells mediated by intercellular disease resistance proteins (R genes) led to effector-triggered immunity (ETI). PTI is generally measured or marked based on ion fluxes, mitogen-activated protein kinase (MAPK) cascades, production of reactive oxygen species (ROS), cell wall reinforcement, pH alkalinization, callose deposition, and defense gene activation mostly regulated by WRKY transcription factors whereas ETI causes visible controlled cell death known as hypersensitive response (HR) (Ingle et al., 2006). Figure 3 illustrates the potential role of the PAMP- and DAMP-mediated defense pathway against P. cactorum. Numerous DAMPs had been identified in plants; however, their roles in plant immunity and defense are not fully understood. Plants could monitor the cuticle integrity and cell walls through DAMPs and activate defense responses. For example, Arabidopsis leaves treated with cutinase or pathogen expressing cutinase gene display strong resistance against necrotrophic fungus Botrytis cinerea (). Oligogalacturonic acid responses were enhanced with overexpression of wall associated kinase 1 (WAK1) and increased resistance to B. cinerea (). Similarly, xyloglucan oligosaccharides act as DAMP and induce immune responses like MAPK activation, callose deposition, and immune gene expression in grapevine and Arabidopsis for resistance against B. cinerea and Hyaloperonospora arabidopsidis (). Additionally, extracellular amino acid histidine acts as DAMP and induces resistance against soilborne bacterial pathogen Ralstonia solanacearum and B. cinerea in Arabidopsis and tomato, respectively, through activation of the ethylene signaling pathway (Seo et al., 2016). Moreover, the genus Phytophthora induces necrosis and immune response in several plant species using cellulose binding elicitor lectin (CBEL). A receptor-like kinase BAK1 (general regulator of basal immunity) is required for CBEL-induced defense responses and respiratory burst oxidase homologue (RBOH)-mediated production of reactive oxygen burst (Larroque et al., 2013). The result showed that a BAK1- and RBOH-dependent CBEL-triggered immunity is important for Phytophthora resistance, whereas susceptibility to Phytophthora does not correlate with natural quantitative variation of basal immunity triggered by conserved elicitors such as CBEL.
Figure 3
Potential application of CRISPR gene editing for the PhCR resistance in strawberry
The Clustered Regularly Interspaced Short Palindromic Repeats (CRISPR)/Cas9 system has been widely applied for targeted gene editing in humans, animals, and plants (Yang et al., 2013; Shalem et al., 2014; Zhang et al., 2014). In plants, genome editing can be used not only for studying gene functions but also in developing new germplasm by inducing mutations or modifying target genes. The method of gene editing has a great potential to enhance the breeding process for improving fruit quality and disease resistance in strawberry (; Yang et al., 2013; Ito et al., 2015). In traditional breeding, the linkage drag is often challenging for the introgression of new resistance traits from wild varieties into elite cultivars. Because certain resistance genes could be genetically linked to loci associated with agronomically important traits such as yield and plant development (Lewis et al., 2007; Miah et al., 2013; Summers and Brown, 2013), modifying target genes precisely using CRISPR-guided mutation could be the effective way to resolve this issue of linkage drag.
The technique of CRISPR/Cas9 has been applied to improve cultivars for disease resistance against soilborne pathogens in plants (Table 1). Mutations in Non-expressor of Pathogenesis-Related 3 (TcNPR3) gene induced by transient expression of CRISPR/Cas9 lead to enhanced defense response to P. tropicalis in Theobroma cacao (). TcNPR3 mutagenesis by CRISPR/Cas9 reduced lesion sizes in CRISPR/Cas9-treated leaf tissues and elevated the expression of pathogenesis-related (PR) genes (). In another study, CRISPR/Cas9-induced mutation in Downy Mildew Resistance 6 (DMR6) enhances defense response to broad-spectrum plant pathogens (Xanthomonas spp., Pseudomonas syringae, and P. capsica) in tomato (). SlDMR6-1 mutagenesis by CRISPR/Cas9 delayed disease progression of P. capsica and the disease symptom was less severe in SlDMR6-1 edited plants (). Furthermore, CRISPR/Cas9-mediated gene editing could precisely repair mutations on target genes by homologous recombination (HR). Single-nucleotide polymorphisms and small InDel mutations of resistance genes could be potential candidates for CRISPR/Cas9-mediated HR applications. With more knowledge on host–pathogen interactions for PhCR resistance, we would have more feasible options for CRISPR-guided resistance breeding to PhCR in strawberry.
Table 1
| Plant | Pathogen | Target gene | Reference |
|---|---|---|---|
| Theobroma cacao | Phytophthora tropicalis | TcNPR3 | () |
| Solanum lycopersicum | Xanthomonas spp., Pseudomonas syringae, and Phytophthora capsica | SlDMR6-1 | () |
| Citrullus lanatus | Fusarium oxysporum | Clpsk1 | (Zhang et al., 2020) |
| Triticum aestivum | Fusarium graminearum | TaNFXL1 | () |
| Gossypium hirsutum | Verticillium dahliae | Gh14-3-3d | (Zhang et al., 2018) |
| Brassica napus | Verticillium longisporum | BnCRT1a | (Pröbsting et al., 2020) |
Applications of CRISPR/Cas9 for improvements of disease resistance to soilborne pathogens.
CRISPR/Cas9-mediated target mutagenesis studies have recently been reported in octoploid strawberry (Xing et al., 2018; Martín-Pizarro et al., 2019; Wilson et al., 2019). Transient assay of CRISPR/Cas9 introduced targeted mutations was performed with FvMYB10 (R2R3 MYB transcription factor 10) and FvCHS (chalcone synthase) genes involved in fruit color development. Agrobacterium-mediated transformation was utilized for the stable integration of CRISPR/Cas9 construct targeting PDS (phytoene desaturase). In addition, the CRISPR/Cas9 gene-editing system was first evaluated for the functional change of gene using Tomato MADS box gene6 (TM6) in the octoploid cultivated strawberry. The tm6 mutant lines exhibited morphological abnormalities in anthers and pollen grains (Martín-Pizarro et al., 2019).
Because of the high complexity of polyploid genome of strawberry, designing a single guide RNA (sgRNA) specific to a target gene is necessary to reduce any off-target effects. The 5’-end 20 nucleotide sequences in sgRNA determine target specificity and potential off-targets. Particularly, 8–12 nucleotides proximal to PAM (seed sequence) have a crucial role in the target gene recognition and cleavage (Jiang et al., 2013). A number of bioinformatic tools are currently available for designing sgRNA in different plant species (Table 2). CRISPOR, CRISPRdirect, CRISPR-P, CRISPR RGEN Tools, and CHOPCHOP provide a genome-wide survey of specific sgRNAs in diploid (F. vesca) and octoploid strawberry (F. ×ananassa). Moreover, CRISPR RGEN Tools and PolyOligo provide designing sgRNA on diploid and octoploid strawberry genomes. The recent haplotype phased genome of octoploid strawberry, FaRR1 (cv. Royal Royce), is now available in CHOPCHOP.
Table 2
| Program | URL | Strawberry genome |
|---|---|---|
| Breaking Cas | http://bioinfogp.cnb.csic.es/tools/breakingcas | N.A.a |
| CCTop | http://crispr.cos.uni-heidelberg.de | N.A. |
| CGAT | http://cbc.gdcb.iastate.edu/cgat | N.A. |
| CHOPCHOP | http://chopchop.cbu.uib.no | Fragaria × ananassa |
| CRISPOR | http://crispor.tefor.net | Fragaria vesca |
| CRISPRdirect | http://crispr.dbcls.jp | Fragaria vesca |
| CRISPR-GEd | http://skl.scau.edu.cn | N.A. |
| CRISPR-P | http://cbi.hzau.edu.cn/CRISPR2 | Fragaria vesca |
| CRISPR-PLANT | https://www.genome.arizona.edu/crispr | N.A. |
| CRISPR RGEN Tools | http://www.rgenome.net | Fragaria vesca Fragaria × ananassa |
| E-CRISP | http://www.e-crisp.org/E-CRISP | N.A. |
| GT-Scan | https://gt-scan.csiro.au | N.A. |
| PolyOligo | http://ec2-52-52-41-39.us-west-1.compute.amazonaws.com/ | Fragaria × ananassa |
List of sgRNA design programs publicly available.
Not available.
Conclusion
The recent genomic advances in both P. cactorum and strawberry have been greatly valuable for the resistance breeding of PhCR in octoploid cultivated strawberry. Because of the availability of high-quality chromosome-scale reference genomes of octoploid strawberry, it could be possible to discover more genes and rare alleles associated with the resistance to multiple pathogens and other important breeding characteristics. Furthermore, genomics research for characterizing gene functions will accelerate to develop gene-specific markers and facilitate the effectiveness of marker-assisted selection in development of new disease-resistant varieties. In new approaches of disease resistance breeding, one of the most exciting prospects would be to discover susceptibility (S) genes using an octoploid strawberry pangenome and utilize them with CRISPR/Cas9-guided mutation tools including a DNA-free gene editing platform suitable for generation of breeding accessions and varieties.
Funding
This work was supported by the Florida Strawberry Growers Association, and Specialty Crops Research Initiative grant no. 2017-51181-26833 from the USDA National Institute of Food and Agriculture.
Publisher’s note
All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article, or claim that may be made by its manufacturer, is not guaranteed or endorsed by the publisher.
Statements
Author contributions
SS, MM, NP, and SL developed ideas and prepared the manuscript. SS, MM, ML, and JB wrote the manuscript, and all the remaining authors contributed to the final version of the manuscript.
Conflict of interest
Author JB completed this manuscript at University of Florida and is now employed by Syngenta Crop Protection, LLC.
The remaining authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.
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Summary
Keywords
DNA marker, marker-assisted selection (MAS), genome assembly, disease resistance (R) genes, CRISPR genome editing, octoploid reference genome
Citation
Sharma S, Marin MV, Lee MB, Baggio JS, Peres NA and Lee S (2022) Genomic approaches for improving resistance to Phytophthora crown rot caused by P. cactorum in strawberry (Fragaria × ananassa). Front. Agron. 4:941111. doi: 10.3389/fagro.2022.941111
Received
11 May 2022
Accepted
21 July 2022
Published
22 August 2022
Volume
4 - 2022
Edited by
Jonathan Spencer West, Rothamsted Research, United Kingdom
Reviewed by
Yunpeng Cao, Chinese Academy of Sciences (CAS), China; Håvard Eikemo, Norwegian Institute of Bioeconomy Research (NIBIO), Norway
Updates
Copyright
© 2022 Sharma, Marin, Lee, Baggio, Peres and Lee.
This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author2(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
*Correspondence: Seonghee Lee, seonghee105@ufl.edu
‡These authors have contributed equally to this work
†Present addresses: Sadikshya Sharma, Department of Plant Science, University of California, Davis, Davis, CA, United States; Juliana S. Baggio, Syngenta Crop Protection, Vero Beach, FL, United States
This article was submitted to Disease Management, a section of the journal Frontiers in Agronomy
Disclaimer
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