Phytophthora rubi(PHYTFU)
EPPO Datasheet: Phytophthora rubi
IDENTITY
Authority: Man in t Veld
Taxonomic position: Chromista: Oomycota: Oomycetes: Peronosporales: Peronosporaceae
Other scientific names: Phytophthora fragariae var. rubi Wilcox & Duncan
Common names in English: root rot of raspberry
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Notes on taxonomy and nomenclature
Phytophthora rubi was originally considered a variety of P. fragariae, which was differentiated only by host preference (Wilcox et al., 1993). However, based on analyses of isozyme profiles and cox1 sequences, that demonstrated the absence of gene flow between both taxa, P. rubi was described as a distinct species (Man in ‘t Veld, 2007). Previously, molecular analysis based on RFLP and AFLP patterns of both varieties of P. fragariae also indicated that they represented two different genetic entities (Stammler et al., 1993; Brasier et al., 1999). More recently, Adam et al. (2020) studied the genome of P. fragariae and P. rubi isolates and identified a different structure between the two species. Although morphologically and physiologically very similar, isolates of P. rubi differ from P. fragariae being highly pathogenic to raspberry (Rubus idaeus), but cause only small amounts of necrosis in strawberry roots (Wilcox et al., 1993). Phytophthora rubi and P. fragariae have identical ITS sequences, but differ across other gene regions such as Btub, HSP90, cox1 and NADH1 and, therefore, they can unambiguously separate using multigene phylogenetic analyses (Jung et al., 2017). Recent genotyping-by-sequencing (GBS) analyses showed low genetic diversity across the Western United States populations of P. rubi. Demographic analyses suggest that populations of P. rubi from the Western United States are the source of pathogen migration to Europe (Tabima et al., 2018).
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EPPO Code: PHYTFU
HOSTS 2022-05-23
Cultivated raspberries are the principal host, but hybrid berries such as loganberries (Rubus × loganobaccus) and tayberries (Rubus fruticosus × R. idaeus) have been found to be naturally infected. However, for tayberries the disease could not be reproduced in inoculation experiments. Some other genera within the tribe Potentilleae, in the family Rosaceae, may be susceptible but have not been tested. Strawberries are not susceptible to P. rubi, which does not cause typical red core symptoms. The potential host range in the EPPO region would be mainly raspberries, including R. idaeus, R. occidentalis and R. idaeus hybrids (Wilcox 1989).
Host list: Rubus fructicosus x Rubus idaeus, Rubus hybrids, Rubus idaeus, Rubus occidentalis, Rubus x loganobaccus, Rubus x neglectusGEOGRAPHICAL DISTRIBUTION 2022-05-23
Phytophthora rubi has a cosmopolitan distribution, although less widespread than P. fragariae. It was first recorded in England and Scotland in the 1930s (Waterson 1937). Since then, the pathogen has spread mainly in western parts of North and South America, and Canada, Central and Northern Europe, and South-Eastern Australia (Converse & Schwartze, 1968; Boesewinkel, 1982; Duncan et al., 1987; Washington, 1988).
North America: Canada (British Columbia), United States of America (California, New York, Ohio, Oregon, Washington)
South America: Chile
Oceania: Australia (New South Wales, South Australia, Tasmania, Victoria, Western Australia)
BIOLOGY 2022-05-23
Phytophthora rubi has similar morphology and growth–temperature relationships to P. fragariae. The optimum temperature for growth is 25°C and the maximum temperature lies between 25 - 30°C. Its growth, at the optimum temperature (2.9 mm/d) and 20°C (2.7 mm/d), is faster than P. fragariae (Jung et al., 2017). Being a homothallic species, it can survive for many years in soil as resistant oospores. When environmental conditions become suitable (wet soil from precipitation or irrigation), pathogen oospores germinate by forming sporangia, which can infect host tissues by direct germination or by release of motile biflagellate zoospores into the soil water. Zoospores are chemotactically attracted by the root tips of the host plant where they penetrate and colonize the root tissues (Duncan and Kennedy, 1989). The pathogen can produce multiple secondary sporangia on infected roots and release zoospores into the soil, and the cycle starts again. Although there are no known natural hosts other than Rubus spp. P. rubi may be able to survive on other rosaceous hosts. Just as with P. fragariae, the rapid build-up and spread of inoculum, the polycyclic nature of the disease, and the production and subsequent survival of oospores are the main factors which make this disease difficult to control and eradicate (Wilcox et al., 1993). Unlike, P. fragariae there are not yet any reports of races.
DETECTION AND IDENTIFICATION 2022-05-23
Symptoms
As with P. fragariae, P. rubi outbreaks often start from small foci, increasing in size, especially down slopes. Symptomatology includes the development of chlorotic, reddish, scorched, or wilted leaves, thin canopies, stunting, reduced cane production, shriveled fruit and reddish-brown root lesions that may extend up into the canes (Stewart et al., 2014). Below ground symptoms may incude discolored, water-soaked necrotic lesions on the roots and crowns, which later results in wilting and dieback of the above-ground canes. Symptoms usually appear on the upper parts of plants that come under stress in late spring or early summer. Some fruiting canes, i.e. canes in their second year, do not break bud; others break bud but their fruiting laterals wilt and dry out before or at fruiting. When the periderm round the bases of these canes is removed the wood underneath is usually discoloured reddish-brown or brownish-black. There is a dearth of young, first-year canes (primocanes); a very early and useful symptom is the absence in spring of a flush of primocanes in the alleyways between the rows of plants. Young canes wilt to give the appearance of a shepherd’s crook. Their foliage becomes bronzed or reddish, long before autumn (premature autumn colouring). Blackish-purple lesions can be also found at the base of many young canes, best seen by removing the periderm, and these can extend for 20-30 cm above soil level. The root systems of affected plants are badly rotten with few white feeder roots, and the thicker roots have internal discoloration often sharply demarcated from white unaffected regions of the root. Root rot symptoms begin early in the growing season and are the most severe in June as fruit begins to ripen. Plant death occurs when enough of the larger roots and canes are girdled. In severe cases, the entire production field may be killed. Several other Phytophthora species have been isolated from raspberries affected by root rot, although plants infected by these other species are rarely as severely affected as those attacked by P. rubi and lack some of its characteristic symptoms, e.g. the blackish-purple lesions on young canes and large oospores restricted to the stele.
Morphology
The pathogen produces oospores in the infected plant tissues, which are easiest to find in young, soft, rotten roots collected from as high up on the base of the cane as possible. Oospores are limited to the stelar region of rotten roots and are very similar to the oospores of P. fragariae, with mature oogonia usually golden-brown, 28-46 µm (mean 39 µm) in diameter with a single aplerotic oospore, 22-44 µm (mean 33 µm) in diameter (Jung et al., 2017). Antheridia are either paragynous or amphigynous. Sporangia are ovoid, ellipsoid, obpyriform, limoniform in shape, ranging 35.6–61.9 µm (mean 50.2 µm) in length and 18.1–37.3 µm (mean 29.3 µm) wide (Jung et al., 2017). Hyphal swellings are elongated, irregular and catenulate. Chlamydospores are not produced.
Detection and inspection methods
The pathogen can be isolated from infected plants tissues, including discolored bases of stems, thick root pieces and fine rootlets using a selective medium for Phytophthora (Montgomerie & Kennedy 1983; Brunner-Keinath & Seemüller 1992). It can be also detected from rhizosphere soil samples collected around symptomatic plants using baiting tests (Erwin & Ribeiro 1995).
Pieces of root, some with young buds attached, are collected in late autumn. They are mixed with a soilless compost and the mixture is used to fill flat planting trays. The trays are kept under good lighting and high temperatures and with just enough water to permit the development of the young buds into vigorous shoots. After about 5 weeks the trays are transferred to cool conditions with moderate lighting and copious watering (care should be taken to ensure that the pots drain freely and do not become stagnant). The new conditions encourage the development of the disease if present, typically wilting and yellowing of leaves, stem lesions and root rot with characteristic oospores in the stele.
Early diagnosis can be made by the detection of small amounts of antigen using an ELISA test. PCR-based detection tests can also rapidly detect the pathogen, particularly if integrated with the baiting method. PCR tests have been developed targeting the internal transcribed spacer region of the ribosomal gene repeat (rDNA) using specific primers in nested PCR (Cooke et al., 1990). Although this method was mainly developed for P. fragariae, it can also be used for P. rubi (Bonants et al., 2004). Rapid, specific and high-throughput sequencing methods may be another opportunity for molecular detection of the pathogen from asymptomatic plants at the control points at import (Liao et al., 2019).
PATHWAYS FOR MOVEMENT 2022-05-23
The movement of infected raspberry planting material as well as infested soil are key means of pathogen dispersal within countries and between fields and regions. For example, Graaberg (1994) suggests that this is how P. rubi was introduced into Sweden. As is the case for P. fragariae, P. rubi can spread in surface water run off or drainage flows, and this can be important for local spread as well as spread from infected tissues to healthy plant tissues by rain-splash. Caution must be exercised when irrigating crops as the pathogen has been spread by irrigating with water which had drained from diseased fields, especially in very wet, mild winters. It can also be moved in soil on implements and machinery.
PEST SIGNIFICANCE 2022-05-23
Economic impact
Phytophthora rubi is the most serious pathogen of raspberry worldwide, and it can result in complete crop losses, as large areas are completely killed (Wilcox and Cooke 2017). To establish raspberry plantations requires considerable capital investment, which is recovered over the life of the plantation, usually 10-15 years. This investment is lost if severe outbreaks occur within 2-3 years of planting. The disease is of great importance in France, Germany, Norway, Switzerland and the United Kingdom. In 2013, P. rubi was found in 90% of the surveyed raspberry fields in Washington state, with the potential of causing millions of dollars in losses to the industry annually (Gigot et al., 2013; Stewart et al., 2014).
Control
Phytophthora rubi is difficult to control, as it overwinters in the soil as oospores that can initiate epidemics in subsequent years. An integrative management approach, including development of resistant raspberry cultivars, fungicides and fumigants, and avoidance of wet soils, is suggested for control of this disease (Wilcox et al., 1999). A number of fungicides such as Mefenoxan (Ridomil) and phoshorous acid (Aliette, Agri-Fos and Rampart) have proved to be effective to control raspberry root rot in USA, although some pathogen resistance maybe develops (Stewart et al., 2014). Applications are made in autumn and spring as band sprays directed at the soil at the base of the canes.
Another management tool is soil solarization, which employs solar radiation to heat soil under a transparent plastic film to temperatures that are detrimental to soilborne pathogens (Pinkerton et al., 2009). Solarization targets mesophilic organisms, which include most plant pathogens and pests, without destroying thermo- tolerant fungi and Bacillus spp. (Pinkerton et al., 2009).
An integrative management approach, including development of resistant raspberry cultivars, fungicide and fumigants, and avoidance of wet soils, is suggested for control of this disease (Wilcox et al., 1999). Planting raspberries on ridges (hilling) is a standard practice worldwide to improve drainage and aeration, and in some soils, improves plant growth and fruit yields (Maloney et al., 1993; Wilcox et al., 1999). Some control can also be obtained by good cultural practices, especially by improving drainage. Heiberg (1995) has proposed an integrated control system, based on raised beds, moderate cultivar resistance, fungicide treatment, mulching and organic amendment. In North America, a number of cultivars have useful levels of resistance: the red raspberries (R. idaeus) Newburgh, Meeker, Sumner (Barritt et al., 1981) and Chilliwack (Daubeny, 1987) have some resistance while Latham and some black raspberry (R. occidentalis) cultivars are highly resistant. Some autumn-fruiting cultivars such as Autumn Bliss appear to have useful levels of resistance, but all summer-fruiting cultivars are susceptible, in most cases extremely so. Rubus spectabilis and R. parviflorus have high levels of resistance (Bristow et al., 1988), and are being used in breeding programmes. The resistance of Autumn Bliss probably comes from R. spectabilis. Most hybrid berries such as tayberry which have blackberry in their parentage are highly resistant or immune, but loganberry is moderately susceptible.
Raspberry genotypes originating from breeding programs around the world have been selected for having high to moderate levels of disease resistance to P. rubi (Pattison & Weber 2005). Direct involvement of antibiotics in biocontrol has been proven in recombinant Streptomyces melanosporofaciens strains developed by intraspecific protoplast fusion (Agbessi et al., 2003).
EPPO Standard PM 4/10 Certification scheme for Rubus describes the production of certified pathogen-tested material (EPPO, 2009).
Phytosanitary risk
Raspberry root rot was a major reason for the introduction of a statutory certification scheme in Scotland in 1982. EPPO Standard PM 4/10 (EPPO, 2009) emphasises the importance of excluding P. rubi and other Phytophthora species from certified raspberry material. In many certification schemes micropropagation is used for rapid multiplication of stocks, and is widely regarded as a safe tool for the provision of healthy planting material (Anderson, 1980). The raspberry pathogen is a potential hazard where soils remain cool and damp for some part of the year. It presents a serious danger to all parts of the EPPO region where raspberries are grown and is still of relatively limited distribution.
PHYTOSANITARY MEASURES 2022-05-23
To prevent the introduction and spread of P. rubi, import requirements for raspberry plants for planting apply worldwide. P. rubi was long considered a variety of P. fragariae, therefore controlling legislation developed for P. fragariae was also intended to be applicable to this pathogen, although the greater capital investment involved in raspberry production, and the losses which raspberry root rot can cause, makes the need for such legislation pressing. EPPO has not yet recommended any requirements for control of P. rubi, though the EPPO recommendations for certification of Rubus planting material (EPPO, 2009) could provide an adequate basis to ensure that raspberry plants imported through this scheme are free from P. rubi. Phytosanitary certificates are required for imported raspberry plants and examination of stocks must be undertaken in most countries where the presence of the disease has become significant.
REFERENCES 2022-05-23
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Bristow PR, Daubeny HA, Sjulin TM, Pepin HS, Nestby R & Windom GE (1988) Evaluation of Rubus germplasm for reaction to root rot caused by Phytophthora erythroseptica. Journal of the American Society for Horticultural Science 113, 588-591.
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Liao F, Huang GM, Zhu LH, Lv D, Zhang D, Luo JF & Li GR (2019). Quadruplex PCR detection of three quarantine Phytophthora pathogens of berries. European Journal of Plant Pathology volume 154, 1041–1049.
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ACKNOWLEDGEMENTS 2022-05-23
This datasheet was extensively revised in 2022 by Bruno Scanu of the University of Sassari (Italy). His valuable contribution is gratefully acknowledged.
How to cite this datasheet?
Datasheet history 2022-06-03
This datasheet was first published in the EPPO Bulletin in 1982 (as Phytophthora fragariae) and revised in the two editions of 'Quarantine Pests for Europe' in 1992 and 1997, as well as in 2022. It is now maintained in an electronic format in the EPPO Global Database. The sections on 'Identity', ‘Hosts’, and 'Geographical distribution' are automatically updated from the database. For other sections, the date of last revision is indicated on the right.
CABI/EPPO (1992/1997) Quarantine Pests for Europe (1st and 2nd edition). CABI, Wallingford (GB).
EPPO (1982) Data sheets on quarantine organisms, Phytophthora fragariae. EPPO Bulletin 12(1), 105-111.
