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Plantwise Technical Factsheet

white rust of crucifers (Albugo candida)

Host plants / species affected
Alliaria petiolata (garlic mustard)
Amaranthus viridis (slender amaranth)
Arabis alpina
Arabis caucasica (snow-in-summer)
Arabis hirsuta (hairy rock-cress (UK))
Armoracia rusticana (horseradish)
Brassica juncea
Brassica juncea var. juncea (Indian mustard)
Brassica napus var. napus (rape)
Brassica nigra (black mustard)
Brassica oleracea var. botrytis (cauliflower)
Brassica oleracea var. capitata (cabbage)
Brassica oleracea var. gemmifera (Brussels sprouts)
Brassica oleracea var. viridis (collards)
Brassica rapa subsp. chinensis (Chinese cabbage)
Brassica rapa subsp. pekinensis
Brassica rapa subsp. rapa (turnip)
Capparis (Caperbush)
Capsella bursa-pastoris (shepherd's purse)
Cleome viscosa (Asian spiderflower)
Daucus carota (carrot)
Eruca vesicaria (purple-vein rocket)
Erysimum cheiranthoides (Treacle mustard)
Erysimum cheiri (wallflower)
Eutrema wasabi (Wasabi)
Ipomoea aquatica (swamp morning-glory)
Lepidium campestre (Field cress)
Lepidium latifolium (perennial pepperweed)
Lepidium sativum (garden cress)
Lepidium virginicum (Virginian peppercress)
Lobularia maritima (sweet alyssum)
Lunaria
Nasturtium officinale (watercress)
Raphanus raphanistrum (wild radish)
Raphanus sativus (radish)
Rorippa amphibia (great yellowcress)
Rorippa islandica (yellow marshcress)
Rorippa sylvestris (creeping yellowcress)
Sinapis alba (white mustard)
Sinapis arvensis (wild mustard)
Sisymbrium altissimum (Tall rocket)
Sisymbrium irio
Sisymbrium officinale (Hedge mustard)
Sisymbrium orientale (eastern rocket (UK))
Spergula arvensis (corn spurry)
Thlaspi arvense (field pennycress)
Tropaeolum majus (common nasturtium)
List of symptoms/signs
Fruit  -  abnormal shape
Fruit  -  galls
Fruit  -  lesions: on pods
Inflorescence  -  distortion (non-graminaceous plants)
Inflorescence  -  galls
Inflorescence  -  lesions; flecking; streaks (not Poaceae)
Inflorescence  -  twisting and distortion
Leaves  -  abnormal colours
Leaves  -  abnormal forms
Leaves  -  fungal growth
Roots  -  galls along length
Seeds  -  shrivelled
Stems  -  galls
Stems  -  mould growth on lesion
Symptoms
Thomas (1984), Kolte (1985), Tewari (1985), Paul and Rawlinson (1992) and Saharan and Verma (1992) have described symptoms on host plants caused by A. candida infection. Symptoms are generally present on above-ground parts of host plants and are of two kinds. The white rust phase (asexual phase) is in the form of raised, milky-white or creamish-coloured single (or coalescing) or concentrically arranged pustules that are closed at first but rupture later and turn powdery-white. The pustules may be present on any above-ground part of the plant including the seedlings but are more common on the underside of leaves. The white rust phase alone results in no or only incipient hypertrophy and hyperplasia of the host tissue and is associated with only limited development of the sexual phase inside the leaf tissue. The leaf area opposite the white rust pustule often bulges out slightly and appears mildly chlorotic but shows chlorophyll retention in the form of a green island as the leaf ages. Harding et al. (1968) studied biochemical and ultrastructural changes in relation to green island formation.

Conspicuous hypertrophy and hyperplasia occurs in parts of the host where the sexual phase of the pathogen develops preferentially. Parts of the inflorescence axes, along with flowers and siliques, swell and curl in various ways resulting in galls known as the 'stagsheads'. These structures are vaguely reminiscent of the heads of stags with antlers, the antlers being represented by pedicles of flowers and siliques. In some cases, isolated flowers and siliques also become malformed. Seeds abort in malformed siliques and contribute to dockage upon harvesting. Terminal parts of the vegetative shoots also sometimes swell and malform. In some cases, parts of the leaves may also curl and twist, but such symptoms are always associated with copious development of the sexual phase in the host tissue. Stem and silique blisters are another symptom of the disease caused by A. candida. Rarely, the roots may also develop galls (Fisher, 1954).

Plant tissues infected with A. candida are also often colonized with a mealy growth of Peronospora parasitica resulting in a disease complex. Field observations indicate that in such cases, most, if not all, hypertrophy of the infected tissue is due to A. candida. Achar (1993) showed that there was no hypertrophy when P. parasitica was inoculated alone, whereas there was hypertrophy when A. candida alone was inoculated. However, there was extreme hypertrophy when both pathogens were inoculated. In addition, Petrie and Vanterpool (1974) reported numerous other fungi also colonizing the 'stagsheads', and stem and silique blisters on Brassica rapa, Camelina microspora and Sinapis arvensis.
Prevention and control
Introduction

Practical strategies commonly used for the management of diseases caused by A. candida include crop rotation, change in sowing date, resistant varieties, clean certified seed and control of volunteer host crop plants and closely related weeds (Barbetti, 1981; Thomas, 1984; Kolte, 1985; Tewari, 1985; Saharan and Verma, 1992; Kharbanda and Tewari, 1996). Early warning systems have so far not been developed for diseases caused by A. candida.

Cultural Control and Sanitary Methods

Oospores, which are the survival and over-seasoning spores of A. candida, are produced in large numbers in the leaves, stem blisters and 'stagsheads'. Consequently, the oospores become crop debris upon harvesting of the crop. Kumar et al. (1995) found white rust development on B. juncea following placement of A. candida inoculum at depths of 7.5 and 10 cm in soil. However, Verma and Bhowmik (1988) were unable to recover any oospores from white rust infested field soil when examined in the following season. Also, they could not recover any oospores from hypertrophied plant parts buried in field soil for 6 months. Hence, they concluded that the soilborne oospores do not play any role in causing primary infections. Collection and burning of infected plants is one of the disease management strategies. However, this approach is only feasible in garden crops, such as cauliflower and horseradish (Armoracia rusticana)(Saharan and Verma, 1992), and not in field crops grown on a large scale. In western Canada, Thomas (1984) recommends a crop rotation of at least 3 years with non-susceptible crops. The oospores are viable even after 21 years of dry storage (Verma and Petrie, 1975). Hence, longer crop rotations may be required for disease control in drier areas of the world (Kharbanda and Tewari, 1996).

Oospores of A. candida can be externally seedborne in large numbers and can serve as a source of primary inoculum (Petrie, 1975; Barbetti, 1981; Verma and Bhowmik, 1988; Randhawa and Aulakh, 1991). Use of clean certified seed is recommended for disease control (Petrie, 1975; Thomas, 1984).

Cruciferous weeds such as Rorippa isladica and Thlaspi arvense harbour races of A. candida that can also infect Brassica rapa (Tewari, 1985). Consequently, control of volunteer crop plants and related weeds is also recommended for A. candida control.

Increasing crop density through the reduction in inter-row and intra-row plant spacing in B. juncea cv. Pusa Bold resulted in increased disease intensity caused by A. candida (Verma and Bhowmik, 1996). Proper seeding practices are, therefore, required for reducing disease severity.

Sowing dates have been shown to have dramatic effects on disease incidence, obviously reflecting changing environmental conditions during different times of the year. Such studies have been carried out in countries such as Australia (Barbetti, 1981), India (Kolte et al., 1986; Tomar et al., 1992; Hegde and Anahosur, 1994) and Iran (Etebarian, 1995) with rapeseed, mustard and cress crops.

Host-Plant Resistance

The histology, biochemistry and genetics of resistance to A. candida has been studied in many brassicas. Histological studies have shown that resistance is expressed only after establishment of the first haustorium of A. candida in the host mesophyll cell (Verma et al., 1975; Liu and Rimmer, 1986; Liu et al., 1989). Several studies have reported a positive correlation between resistance to A. candida and a higher content of phenolics and cholorophyll a and b in B. juncea (Bhatia et al., 1994; Yadav et al., 1996; Gupta et al., 1997). Singh et al. (1998) reported that the resistant genotypes of B. juncea contained higher levels of phenols, orthodihydroxy phenols, flavonoids, total cholorophyll content and exhibited increased deposition of leaf surface waxes relative to controls. However, the flavonoids showed a greater association with resistance relative to other biochemical traits.

There are many known sources of resistance. Resistance to A. candida in crucifers is race specific. In view of the economic importance of Brassicas and of the white rust and 'stagshead' diseases, numerous sources of resistance have been identified in various crops. There are several phenotypic expressions of resistance to A. candida on crucifers. These include no visible symptoms, hypersensitive reaction and very discrete weakly sporulating pustules, mainly on the adaxial surface of cotyledons (Williams and Pound, 1963).

Resistance in brassicas to A. candida is conditioned by up to three dominant or many minor genes (Williams and Pound, 1963; Delwiche and Williams, 1981; Edwards and Williams, 1987; Tiwari et al., 1988; Verma and Bhowmik, 1989; Liu and Rimmer, 1991; Paladhi et al., 1993; Rao and Raut, 1994; Subudhi and Raut, 1994; Ferreira et al., 1995; Liu et al., 1996). Both dominant and additive gene effects are involved in some hosts. Williams and Pound (1963) found that the hypersensitive reaction to A. candida race 1 in radish cv. China Rose Winter may be modified to a weakly sporulating tolerant reaction by environmentally controlled minor genes. Ferriera et al. (1995) reached similar conclusions through their study on B. napus using molecular markers and field testing. Yadav et al. (1994) using field testing found that in B. juncea additive gene effects were more important than dominance effects in the inheritance of resistance to A. candida.

Somaclones constitute additional sources of resistance to A. candida in B. juncea (Katiyar and Chopra, 1990; Sharma and Singh, 1995). Wild and cultivated genotypes of related genera of crucifers are also sources of race specific resistance to A. candida that can be used for brassica improvement (Bansal et al., 1997).

Biological Control

There are no biological control methods for A. candida. However, Pseudomonas syringae is reported to cause soft rotting of the green 'stagshead' caused by A. candida on brassicas (Tewari et al., 1998). This is a form of natural biological control of A. candida, as the developing oogonia and antheridia abort upon soft rotting by this bacterium (Tewari et al., 1998). This bacterium is also known to infect healthy leaves and siliques of Brassica rapa and B. napus, but is especially virulent on the 'stagsheads'. However, cultivars of B. rapa and B. napus currently grown in Canada are especially tolerant to this bacterium in the field. Pending further research, this has raised possibilities that it may be possible to use this bacterium for biological control of A. candida.

Chemical Control

Due to the variable regulations around (de-)registration of pesticides, we are for the moment not including any specific chemical control recommendations. For further information, we recommend you visit the following resources:

Impact
Introduction

A. candida causes economically significant yield and quality losses in seed and vegetable produce of crucifers in several different ways. White rust disease on the foliage reduces the photosynthetic capacity of plants and affects yield and normal plant development. Disease on the foliage affects and downgrades the leaves for sale and its human consumption as a vegetable. The stem blisters caused by the fungus weaken the stem, predisposing the plant to wind damage. Most seed yield reductions are attributed to the staghead phase of the disease in which the whole inflorescence axis becomes hypertrophied and malformed causing a significant nutrient sink effect on the plant. Sometimes only individual flowers and siliques are hypertrophied and malformed. The infected siliques produce only abortive seeds. In a field experiment in Canada with crops sown at different times, Harper and Pitman (1974) studied the relationship between intensity of staghead production and seed yield of Brassica rapa and developed an equation (% yield loss = 0.952 X percent stems with stagheads) for assessing yield losses in the field. It was suggested that for estimating yield loss in commercial crops, the coefficient can be rounded to unity, thus, the simple equation, yield loss (%) = percent stems systemically infected, is produced.

Seeds of susceptible crucifers are commonly infested with oospores of A. candida. It has also been shown that the seeds of some crucifers may carry internal infection by A. candida (Sharma et al., 1997; Jacobson et al., 1998). Use of such seed may initiate epidemics early in the season and may lead to dispersal of different races of the pathogen. Seed infection/infestation relative to A. candida should be important in the economics of certified seed production but it is currently (July 2000) not routinely monitored for seed and crop health management of crucifers.

The host range of A. candida extends mostly to numerous members of Brassicaceae, only some of which are economically important. The economically high profile members of Brassicaceae that are appreciably affected by A. candida include the oilseed (Brassicas, Camelina sativa, and Eruca sativa), vegetable (oleraceous Brassicas, Chinese and Japanese leafy Brassicas, Armoracia rusticana, Raphanus sativus), and some established or emerging industrial crops (C. sativa and Lunaria annua).

A. candida, especially the staghead phase, is generally associated with Peronospora parasitica in the field. In such cases, it is hard to precisely estimate the loss caused by each pathogen. In addition, several other pathogens of crucifers may also be present on the same plant.

India and Pakistan

A. candida has a worldwide distribution but is of significant economic importance only in certain countries on certain crops. India has a huge acreage of susceptible B. juncea and some other oilseed crucifers and is the world's hottest spot for the disease caused by A. candida. The disease is rampant on various crucifers all over India, especially on the oilseed types in the central and northern plains. Saharan and Lakra (1988) and Lakra and Saharan (1989) reported from Haryana, India, that the highest leaf and staghead phase infections in B. juncea cv. Prakash resulted in yield losses of 27.4 and 62.7%, respectively, while the combined infection by these two phases resulted in a yield loss of 89.8%. The various parameters contributing to yield, such as the number of branches/plant, number of siliques/branch, silique length, number of seeds/silique, 1000 grain weight, and total yield/plant were all affected by each category of infection (Saharan and Lakra, 1988; Lakra and Saharan, 1989; Saharan and Verma, 1992). Lakra and Saharan (1989) suggested the prediction equation:

Yield loss (%) = a1x1 + a2x2

where a1 = 0.437 and a2 = 1.176 are constants, and x1 and x2 are disease indices on leaf and staghead phases, respectively.

Bisht et al. (1994) reported yield reduction from 2.4-20.6% due to the staghead phase alone in a susceptible genotype of B. juncea in Delhi, India. Chauhan et al. (1999) showed that the average (1994-98) seed yield of an A. candida-resistant variety of B. juncea (NDM 87-1) in Uttar Pradesh was 1095 kg/ha compared with 855 kg/ha in the popular susceptible control variety Varuna. Yield losses from 21.3-37.2% in B. juncea were reported from Manipur in north-eastern India (Singh et al., 1990). Hegde and Anahosur (1993) reported that seed treatment and foliar sprays with metalaxyl resulted in 94 and 96% reductions in leaf and floral infections, respectively, and an 81.3% yield increase in B. juncea in Karnataka, India. Similarly, there are many more reports of severe economic damage in oilseed crucifers due to A. candida from the aforementioned and other areas of India.

Bains and Jhooty (1979) studied mixed infections of Chinese mustard (B. juncea) with A. candida and P. parasitica in Punjab and reported infections of 0.5-29% during the years 1975-78. The infected plants produced fewer siliques (37-47%) and less seed (17-32%). The disease is important on R. sativus as well, both in northern and southern India (Gupta et al., 1977; Sharma, 1983). Severe infection of Lepidium sativum by A. candida is reported from the Kumaun Himalayas in India (Melkania and Upreti, 1981).

The disease is also common in some other parts of the Indian subcontinent. Jalaluddin et al. (1993) reported that A. candida was common on rapeseed and mustard in Sindh, Pakistan. In Oceania, yield losses of 5-10% due to stagheads in rapeseed were reported from Australia (Barbetti, 1981; Saharan and Verma, 1992).

Europe

The disease caused by A. candida appears to be uncommon on spring oilseed rape in Scotland in the UK (Coll et al., 1998). However, high levels of infection by A. candida have been recorded on Brussels sprouts in the UK (Appleton, 1979). Lunaria annua hosts A. candida in Europe in regions such as England (Cromack, 1998), the Netherlands (Mastebroek and Marvin, 2000), and in Crete, Greece (Vakalounakis, 1991). It causes a serious disease of L. annua in Crete and may reduce seed yields in The Netherlands. A. candida also causes an economically important disease of A. rusticana in countries such as Poland (Macias, 1996), Austria (Szith and Furlan, 1979), and Germany (Kalchschmid and Krause, 1976), and of E. sativa in Italy (Minuto et al., 1997). A. candida has also been recently reported on C. sativa from Germany (Föller et al., 1998).

Middle East

In Iran, 8-47% of cress plants and 8-27% of radish plants (grown for seed) were reported to infected by A. candida (Etebarian, 1993).

North America

In Canada in 1979, A. candida was cited as being the most important pathogen of B. rapa (Verma and Petrie, 1979). In Saskatchewan, Canada, seed yield losses due to the staghead phase during 1970, 1971 and 1972 were estimated to be 0.747 (3%), 1.836 (6%), and 1.08 (9%) million bu, respectively (Petri, 1973). These losses were worth 1.68, 4.13 and 2.43 million dollars, respectively. The estimated yield losses in rapeseed in northern and central Alberta, Canada were 1-2% in 1971 (Berkenkamp, 1972; Saharan and Verma, 1992). In Manitoba, Canada, losses in rapeseed attributed to A. candida in 1971 amounted to 30-60% (Bernier, 1972). During the 1970s the disease on rapeseed rose sharply in severity in the Canadian prairies and yield losses of up to 60% were reported in Saskatchewan, Canada (Saharan and Verma, 1992). However, the disease became unimportant later due to widespread use of resistant cultivars (Petri, 1985a). In 1982, A. candida occurred in 71.4% of B. rapa fields but its incidence of 24.6% was relatively low (Petri, 1985b). Since then, there has been a resurgence of this disease due to the evolution of new races of the pathogen (Petri, 1994). A. candida has also been recently reported on C. sativa from Alberta, Canada (Paul et al., 2000).

Recently, damaging outbreaks of A. candida on the leafy vegetable crucifers B. rapa subsp. nipposinica and on B. rapa subsp. narinosa have been reported from California, USA (Koike, 1996). There is also a recent report of this pathogen on E. sativa from California (Scheck and Koike, 1999).

Related treatment support
 
External factsheets
Department of Agriculture and Food Western Australia Farmnotes, Government of Western Australia, 2006, English language
PlantVillage disease guide, PlantVillage, English language
Aberaeron Allotment Association Fact Files, Aberaeron Allotment Association, English language
Department of Agriculture and Food Western Australia Farmnotes, Government of Western Australia, 2006, English language
PlantVillage disease guide, PlantVillage, English language
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