Egypt. J. Exp. Biol. (Bot.), 5: 1 – 20 (2009) © The Egyptian Society of Experimental Biology

REVIEW ARTICLE

Abdellah Akhkha

Barley Powdery Mildew ( Blumeria graminis f.sp. hordei ) : Interaction, Resistance and Tolerance

ABSTRACT : In the present review, the effect of 1. The importance of barley as a crop and powdery mildew ( Blumeria graminis f.sp. the economic significance of barley mildew hordei) on growth, physiology and metabolism (Blumeria graminis f.sp. hordei ) of barley crop ( Hordeum vulgare ) is discussed. Barley ( Hordeum vulgare ), a small-grain Furthermore, the interactions between the host cereal, belongs to the tribe Hordeae of the (barley) and the pathogen ( B. graminis ) are family Gramineae. It is a major world crop and reviewed in details. Different types of ranks as the most important cereal after rice, resistance including, complete and partial wheat and maize (Bengtsson, 1992). Barley is resistance were discussed. Plant tolerance of widely cultivated, being grown extensively in diseases was also presented in details as one Europe, around the Mediterranean rim, and in of the alternatives to protect crops from Ethiopia, Russia, China, India and North damage caused by the pathogen or the America (Harlan, 1995). In Britain, barley has disease. However, this phenomenon would not been the crop with the largest land acreage for involve pathogen limitation and the pathogen a considerable period of time and still would not affect the crop in a way other represents today, together with wheat, one of intolerant crops would do. The use of the major crops. tolerance in integrated disease management is It has been suggested that cultivated discussed. barley originated from the wild barley,

Hordeum spontaneum C. Koch, which has its

centre of origin in the Fertile Crescent of the

Middle East (Zohary, 1969), with scattered

stands over a much wider area from Tunisia to

Afghanistan and with doubtful occurrence in

Morocco and Abyssinia.

The fungus Blumeria graminis (DC.) KEY WORDS: Powdery mildew, Erysiphe, Speer f.sp. hordei Marchal (Syn. Erysiphe Blumeria, Wild barley, cultivated barley, Hordeum graminis DC. f.sp. hordei Marchal) causes vulgare, Hordeum spontaneum , Resistance and powdery mildew, the most important disease of Tolerance. barley throughout the world where the crop is grown (Bennet and Scott, 1971). The importance of powdery mildew on barley was recognised at the beginning of this century when the disease was observed to cause economic losses (Wolfe and Schwarzbach, 1978). Since then barley mildew has remained a constant problem in many parts of the world, including Europe. For example, annual losses of about 9% are reported in England and Wales (King, 1972 & 1977), 25% in USA (Schaller, 1951) and 30% in North Africa (Yahyaoui et al ., 1997). Even CORRESPONDANCE: greater yield reductions have been found in Abdellah Akhkha experimental studies and losses in grain yield * Division of Biochemistry and Molecular Biology, in excess of 50% have been reported (Rea and Institute of Biomedical and Life Sciences, The Scott, 1973). Bower Building, University of Glasgow, Glasgow G12 8QQ, Scotland, UK. 2. Interactions between barley and B. + Department of Biology, Faculty of Science, graminis f.sp. hordei Taibah University, Madinah, Kingdom of Saudi The responses of barley to infection by Arabia B. graminis have been found to be extremely E-mail: [email protected] varied. Some cultivars may be highly ARTICLE CODE: 01.02.09

ISSN: 12895-2007 http://www.egyptse b . o r g 2 Egypt. J. Exp. Biol. (Bot.), 5: 1 – 20 (2009) susceptible and support high levels of fungal because resistance provides the cheapest and development resulting in the death of the host, the most effective means of controlling while others may be immune. In between the pathogens, particularly powdery mildews of two extremes there is a continuous range of cereals. However, the cultivation of resistant cultivars which support all levels of fungal cultivars on a large scale imposes a strong development (Jones and Clifford, 1983a). selection pressure on the pathogen population for virulent races that can overcome the 2.1. Host resistance resistance. In general, major gene resistance Resistance of a host to a parasite is remains effective for only a few years before a defined by Agrios (1997) to be the ability of the virulent race of the mildew pathogen arise host to prevent, completely or in some degree, which can overcome the resistance. This was the growth and development of that parasite. first observed in the case of the major Different types of resistance in barley to resistance gene Ml-g, which was introduced infection by B. graminis f.sp. hordei have been into European barley varieties in 1930s (Wolfe noted from complete resistance to varying and Schwarzbach, 1978). For example in levels of partial resistance. Germany, when the area under cultivation with 2.1.1. Complete resistance cultivars with Ml-g gene was still small during In many instances, complete or near the 1930s and 1940s, it remained effective. complete resistance has been found to be However, when areas under cultivation in the controlled by one or at most two or three late 1940s started to increase rapidly, this genes with major effect. This type of resistance gene was defeated (Wolfe and resistance is often called race-specific Schwarzbach, 1978, Wolfe, 1984). The resistance or major gene resistance and is instability of major gene resistance has caused often expressed as a hypersensitive reaction plant breeders to look for ways to use it, which (Jones, 1987). might make it more durable. The specificity of most types of major Three methods have been used to gene resistance suggests that there is some improve the durability of major gene relationship between specific avirulence genes resistance, pyramiding resistance genes, in the different physiologic races of the multiline varieties and variety mixtures. pathogen and the different resistance genes in Pyramiding resistance genes consists of the host cultivars incorporating them. breeding as many of the genes as possible into a cultivar before releasing it into commercial Many B. graminis f.sp. hordei avirulence production. This means that the parasite must alleles and barley resistance genes were found overcome all the resistance genes before it to follow a gene-for-gene relationship, a becomes virulent. relationship which was first demonstrated by Flor in 1956 between flax and flax rust Multiline varieties are formed as (Moseman, 1957and1959). combinations of isogenic lines, identical in all agronomic characters but differing in the race- The application of Flor’s gene-for-gene specific resistance gene they contain (Jones hypothesis has facilitated the identification of and Clifford, 1983b, Manners, 1993). In order specific resistance genes in barley and their to break down the resistance of the multiline, corresponding pathogenicity genes in B. the pathogen must acquire enough different graminis f.sp. hordei. In this way, a large virulence alleles to overcome all the resistance number of resistance genes in cultivated genes present. barley and wild species of barley have been identified and mapped (Wolfe, 1972, Giese, Variety mixtures consist of several 1981, Giese et al ., 1981, Søgård and varieties, which are similar to each other in Jørgensen, 1987). agronomic characters, but which have different resistance genes. Mixed varieties have been Resistance to at least some variants of shown to have reduced levels of infection and B. graminis f.sp. hordei is determined by consequently reduced yield loss of the alleles located in at least seven loci. At least individual components of the mixture, when five of these loci appear to be located on the compared to the mean yield from pure stands long arm of chromosome 5, whereas the other (Wolfe, 1985). However, mixed varieties, like two loci, Ml-g and Ml-o, are located on multiline varieties and pyramiding, could lead chromosome 4 (Wolfe, 1972). The resistance to the development of new and more virulent alleles are designated after the cultivar or line races (super-races) that are virulent on all of in which they were first identified; eg. Ml-a (cv. the varieties in the mixture (Groth, 1976). This Algerian), Ml-at (cv. Atlas), Ml-g (cv. Goldfoil), possibility was supported experimentally by the Ml-h (cv. Hanna), Ml-k (cv. Kwan), Ml-p (cv. work of Huang et al . (1994) who suggested Psaknon) and Ml-o (McIntosh, 1978). that super-races would dominate a mildew Plant breeders produce new resistant population when the same cultivar mixtures or cultivars by incorporating single major genes multilines were used continuously over long derived from Hordeum spontaneum . These periods and large areas. The search for more resistant cultivars are extensively used, durable forms of resistance should continue. particularly in Europe and North America, 2.1.2. Partial resistance

ISSN: 12895-2007 http://www.egypts e b . o r g Akhkha A., Barley Powdery Mildew ( Blumeria Graminis F.Sp. Hordei): Interaction, Resistance … 3

Many barley varieties have been found to have stable tolerance which was expressed in be partially resistant to B. graminis pathotypes. each season, while others expressed unstable Such varieties support the growth of the tolerance which was expressed in one season fungus but the growth is limited. Partial but not in another. resistance tends to be more durable than race Simon (1966) examined 24 oat cultivars specific resistance (Roberts and Caldwell, for their reactions to crown rust ( P. coronata ) 1970). It is in fact not specific and affects and concluded that cv. Cherokee and several several of the pathogen infection processes, other cultivars with susceptible reactions were pathogenicity and sporulation. It is believed to significantly more tolerant of given levels of be controlled by a number of genes each with infection, as measured by kernel weight ratio, small effect (Parlevliet, 1981) and it is than cvs Clinton and Benton. sometimes referred to as polygenic resistance However, in none of these cases, were (Asher and Thomas, 1987). Partial resistance the rates of development of parasite biomass is more durable because the pathogen has to and or disease examined. Clarke (1986) undergo several genetic changes to overcome concluded that none of the studies clearly the resistance (Jørgensen, 1994). established that the named cultivars were Partial resistance has been transmitted really more tolerant of infection than some of to new varieties in breeding programs (Roberts the other cultivars with which they were and Caldwell, 1970). Unfortunately, this type of compared. In contrast, the experiments carried resistance rarely provides an adequate level of out on oat plants by Sabri et al. (1993, 1995 resistance. It is also difficult to evaluate its and 1997) in which reductions in host plant level in the field without growing the plants to growth and changes in photosynthesis and maturity and it is more difficult than major gene respiration were related to parasite biomass resistance to manipulate in breeding programs development, gave results which clearly (Jones, 1987). However, if supported by other showed that one cultivar cv. Lustre was more control measures, such as the use of tolerant of given levels of mildew infection than fungicides, it can give useful mildew control. another, cv. Peniarth. Furthermore, Akhkha et Since partially resistant cultivars are al. (2003a) reported that a wild barley line was susceptible in wild populations, genotypes more tolerant to infection by Blumeria graminis which are least affected by that level of f.sp. hordei than two cultivated barley infection are likely to have the higher cultivars. In addition, Akhkha et al . (2003b) reproductive output and thus have a selective showed that the physiology of the same wild advantage over genotypes which are affected line was less affected than the other two more. Genotypes which are least affected are cultivars. the most tolerant genotypes and thus tolerance 2.2.2. Evidence for tolerance in native is likely to play a significant role in a host’s plants survival strategy and could be used as a crop It has been commonly observed (Tarr, protection measure. 1972) that some wild plants can be very 2.2. Tolerance of the parasite susceptible to a parasite yet appear to be little Tolerance of the parasite in plants is affected by it. This general view that wild defined as the ability of a plant to endure the plants may be more tolerant of parasitic effects of levels of parasitic development, infection than cultivated plants gained some which if they occur at equivalent levels in other support experimentally from the work of Ben- plants of the same or of similar species would Kalio and Clarke (1979) on the effects of the cause greater impairment of growth or yield powdery mildew fungus Erysiphe fischeri on (Clarke, 1986). the growth and development of Senecio 2.2.1. Evidence for tolerance in crop plants vulgaris (groundsel). They observed that up to 30% mildew cover had no effect on plant That some cultivars of some crops may growth. Even heavy levels of infection, when vary in their tolerance of infection has been up to 75% of total leaf area were colonised, did suggested for many years. One of the first not effect chlorophyll levels in the leaves nor reports of tolerant cultivars in cereals is that of the rate of dry-matter production per unit area Salmon and Laude (1932). They claimed that of leaf, and nor did they affect photoassimilate Fulhard wheat was more tolerant of leaf rust distribution between the different parts of the (P. recondita ) than were other cultivars used in plant. However, leaf expansion was reduced a trial. These results were verified and and so total plant growth and number of supported by Caldwell et al . (1934). flowers and fruits were reduced. Newton et al. (1945) compared the Similarly, comparative studies of the reactions of six barley cultivars to leaf rust ( P. effects of powdery mildews on willow herb hordei ) and concluded that two cultivars (Epilobium montanum ) and couch grass (Mensury and O.A.C.21) were more tolerant (Elymus repens ) indicated that infection did not than the other four cultivars. Similarly, Kramer reduce growth until more than 30% of the et al . (1980) compared the reactions of fifteen aerial surfaces were colonised (Clarke, 1988). spring barley cultivars to leaf rust ( P. hordei) Levels of infection above 30% progressively and observed that some cultivars appeared to reduced growth but to a lesser extent

ISSN: 12895-2007 http://www.egypts e b . o r g 4 Egypt. J. Exp. Biol. (Bot.), 5: 1 – 20 (2009) compared to crop plants such as cereals, percentage mildew cover, was about 30%. where growth is generally depressed Infected plants also produced shorter primary substantially even by low levels of infection shoots, fewer shoots per plant and developed (Ayres, 1984). a smaller leaf area per shoot than the More recently, Sabri (1993) and Sabri et uninfected controls. The reduced dry weight of al . (1995) compared the effects of B. graminis the shoot system of infected plants was found f.sp. avenae on the growth of one wild line of to be closely paralleled by a reduced leaf area. oat ( Avena fatua ) and two cultivated oats During the early stages of infection, reduced Lustre and Peniarth ( A. sativa ) and found that growth was attributed mainly to fewer shoots although the wild oat supported the highest per plant, but later, also to reductions in total levels of mildew development, its growth and leaf area as well as to fewer shoots. The mean yield were reduced less than those of the two unit leaf rate or net assimilation rate was also cultivated oats particularly cv. Peniarth. Thus reduced by infection, by about 27% compared the wild line appeared to be much more to the uninfected plants. Unexpectedly, tolerant of given levels of mildew infection than infection reduced root growth more than shoot either of the two cultivated oats particularly cv. growth. The reductions in leaf area, net Peniarth. assimilation rate and root growth were reflected in smaller grain yields, due to the Since reductions in growth were due to production of smaller and fewer ears. The the effects of mildew infection on leaf average decreases in dry weight per ear and in development and function, Sabri (1993) and number of ears per infected plant were about Sabri et al . (1997) investigated the effects of 21% and 12%, respectively. infection on photosynthesis and respiration in the three oat lines. The results indicated that Although Paulech (1969) obtained similar gross and net photosynthesis and chlorophyll results to Last, the results of both workers levels were reduced by infection in all three were open to criticism for three reasons. lines, but to the greatest extent in cv. Peniarth, Firstly, the experiments were carried out in to a lesser extent in cv. Lustre and to the least glasshouses where mildew developed more extent in the wild oat despite the latter severely than in the field. Secondly, plants supporting the development of the highest were grown in pots and so may be qualitatively level of mildew biomass. This study supported and quantitatively different from those grown in the results of the growth analysis that wild oat the field. Thirdly, the effects on growth depend possessed more tolerance of infection than on the growth stage at which infection occurs either of the two cultivated oats. It was also (Brooks, 1972). found that for given levels of mildew biomass Working with spring barley in field trials, development, cv. Lustre was less affected than Brooks (1972) found that the growth and yield cv. Peniarth indicating that cultivars may differ of winter barley, which can be subject to in their tolerance. Akhkha (2003b) investigated severe mildew attack in both autumn and in also the effects of powdery mildew on the spring, was significantly reduced. He observed growth, development, photosynthesis and that when an early and severe attack was respiration in wild and cultivated barley lines. contained for the whole season, there was He concluded that a wild barley line (B19909) about 26% increase in the yield because of the was more tolerant than any other lines increased numbers of fertile tillers produced although it showed the highest level of and the increased ear weight. When mildew infection. infection occurred late in plant development, From these studies on tolerance of wild reductions in grain size were the only effect. In relatives, it was concluded that wild plants general, Brooks (1972) confirmed the might possess higher levels of tolerance of observations on pot grown plants made by Last parasites than crop plants. (1962) and Paulech (1969). 3. How pathogens affect the growth and Griffiths et al . (1975), in pot experiments, yield of susceptible hosts investigated the effects of mildew epidemics of different duration and with varying times of 3.1. Effects on the shoot growth and yield inoculum arrival on grain production. They Detailed growth analysis on some showed that an early mildew attack not only important crop species has been carried out to reduced tiller number but also grain size and investigate just how pathogens affect the number of grains per tiller, but late mildew growth and development of the plant. attack reduced only the number of fertile tillers In glasshouse experiments, Last (1962) with no significant effect on grain size or studied the effects of B. graminis f.sp. hordei number. The change in the plant response to on the growth and development of spring mildew infection was found to occur about G.S. barley plants. He showed that although total 5.0, i.e. at the end of tillering, but after this plant dry weight of infected plants continued to stage, the effect of mildew epidemics on increase, final dry weights were reduced by tillering was much reduced. This was due to about 59% compared to the uninfected controls the fact that tillering in barley is completed at by 11 weeks after inoculation. At this stage the G.S. 3.0 (Zadoks et al ., 1974). mean level of infection, measured as These studies were confirmed and

ISSN: 12895-2007 http://www.egypts e b . o r g Akhkha A., Barley Powdery Mildew ( Blumeria Graminis F.Sp. Hordei): Interaction, Resistance … 5 investigated in more details by Scott et al. water and nutrients and transport these to the (1980) who found that significant reductions in shoots together with certain plant growth grain number and size could occur even with regulators that they synthesise (Ayres, 1984). late mildew attack because of the effects of The growth and physiological efficiency of infection on photoassimilate production during cereal roots can be disrupted directly by root the period of grain filling. parasites (Asher, 1972, Clarkson et al ., 1975, The greatest effect of mildew is to Fitt et al ., 1978) or indirectly by foliar parasites accelerate leaf senescence so that green leaf such as powdery mildew (Last, 1962, Paulech, area (GLA) is reduced (Last, 1962). Many 1969, Walters and Ayres, 1981a). studies have revealed close relationships Last (1962) was the first to note that between GLA or GLA duration and crop yield mildew infection of the leaves reduced root losses (Rea and Scott, 1973, Jenkyn, 1976, growth relatively more than shoot growth. He Carver et al ., 1981and1982, Lim and Gaunt, found that root dry weight per unit leaf area 1986, Waggoner and Berger, 1987). For was decreased in infected plants by up to example, Carver et al . (1981) examined the about 32% of the level in uninfected plants. He relationships, using greenhouse grown barley suggested that some of the efficiency of the plants, between the severity of powdery assimilatory apparatus could be affected by mildew, green leaf area (GLA) and grain yield. the large reductions in the absorbing systems The results showed that mildew reduced GLA (roots). Paulech (1969) and Brooks (1972) in proportion to its severity and there was an confirmed that roots were affected more than almost complete correlation (r = 0.99) between shoots by mildew infection in barley plants. GLA and grain yield in both primary shoots and The branching pattern of roots was also tillers. There was also a good correlation found to be affected by mildew infection. between disease progress and total yield of Vizárová and Minar čic (1974) observed that in primary shoots (r = 0.95). Detailed analyses of barley plants, four days after inoculation with the data indicated a dominant role for GLA pre- B. graminis f.sp. hordei , the rate of elongation anthesis on grain yield associated with mildew of the seminal roots was reduced as also was epidemics. GLA before anthesis determined the growth and formation of lateral roots. They the amount of stored photosynthate generated also noticed that the diameters of the roots before anthesis and available for were smaller and thus that the roots had a retranslocation to the developing grain. much smaller stele than the roots of healthy However, field-grown plants generally plants. Minar čic and Paulech (1975) also differ from those grown in the glasshouse in observed this reduction in the stele size. the development of smaller leaves due to the More detailed investigations of the effects of temperature and light intensity effects of mildew on the growth of barley roots (Carver et al ., 1982) and so it is important to were carried out by Walters (1981) and Walters establish whether the responses of field grown and Ayres (1981a). They observed that total plants to mildew attack are similar to those of root dry weight, total root length, as well as the glasshouse grown plants. For this reason, length of individual roots (seminals, nodals, spring barley plants, cv. Julia, were grown in and laterals) were significantly decreased by micro-plots in the field (Carver et al ., 1982), mildew infection. The numbers of seminal and but the observations from these field nodal roots were not affected by infection but experiments confirmed almost all the details there was a significant reduction in the number gained from greenhouse experiments (Carver of primary and secondary laterals formed by et al ., 1981). both types of roots. Reduced stele size was In contrast to the findings of Carver et al . also reported which was in agreement with the (1981and1982), that late mildew epidemics had results of Vizárová and Minar čic (1974) and only small effects on grain yield, Wanzhoug Minar čic and Paulech (1975). The results (1988) using cv. Triumph, observed that presented by Walters (1981) showed that although early mildew attacks were more mildew infection lead to a reduction in the damaging to plant growth and yields than late number and size of the inner metaxylem attacks, late epidemics also caused significant vessels and in the size of the endodermis. losses in most yield components. The The effects of mildew infection on mitotic difference in yield responses to late mildew cell division in the apical meristems of the epidemics found between Carver et al .’s (1981) roots of barley plants were first investigated by and Wanzhoug’s (1988) experiments may be Minar čic and Paulech (1975). They observed explained by different degrees of tolerance that infection reduced mitotic cell division in between the cvs Julia and Triumph or by the apical root meristems of a highly differences in environmental conditions. susceptible barley cultivar in response to 3.2. Effects on root growth and physiology mildew infection and Walters (1981) obtained The effects of powdery mildews and similar results. Lewis and Deacon (1982) other foliar pathogens on plant growth were investigated the effects of mildew infection on usually considered in relation to the leaf the senescence of the root cortex of barley environment and little thought was given to seedlings, but found little difference from possible effects on root growth. Roots take up uninfected plants. Last (1962) suggested that

ISSN: 12895-2007 http://www.egypts e b . o r g 6 Egypt. J. Exp. Biol. (Bot.), 5: 1 – 20 (2009) the reductions in the root systems in barley From all the studies presented here, it is caused by mildew infection was a secondary clear that the roots of barley are significantly effect of the lower unit leaf rates, but a stage altered morphologically, anatomically and may, however, be reached when the smaller physiologically by infection with powdery root system itself affects leaf efficiency. Fric mildew fungi. These changes must have a (1975), attributed effects on root growth to the detrimental effect on the growth of the plants reduction in the quantity of photoassimilates and thus on yield. reaching the root, but he also suggested that 3.3. Functional equilibrium between roots other factors might be responsible such as and shoots of infected plants disturbances to the hormonal balance of the Shoots, together with the roots, roots. Vizárová and Minar čic (1974) in fact constitute the entire plant structure and the found that treatment of healthy barley with root: shoot ratio can provide an index of the cytokinin did result in alterations in the root performance of each organ in a given growth system which were similar to those observed in environment. mildewed plants. Thus, the increase in cytokinin levels detected around four days Based on the work of Davidson (1969) after inoculation in infected plants may be and Thornley (1972), several workers have associated with the morphological changes demonstrated a functional equilibrium between observed in the roots. However, the level of root and shoot growth and the development of cytokinins was observed to decrease later and uninfected plants (Richards, 1977&1978). thus effects on root growth must be due to Ayres (1984) suggested that the equilibrium other factors. The reduction in the mitotic cell between root and shoot growth is mediated by division of the root apices may also be water and nutrients moving from root to shoot, attributable to a decreased photoassimilate by photoassimilates moving from shoot to root supply from the shoots to the roots (Minar čic and by growth regulators moving in both and Paulech, 1975) and such a reduction was directions. However, it was mentioned earlier later reported by Walters (1981) who observed that the dry weights of the roots of barley a reduced supply of 14 C photoassimilates to plants infected with B. graminis f.sp. hordei the root tips of infected plants. were reduced more than shoot dry weights and consequently, the root : shoot ratio had been Undoubtedly, the changes in root decreased by infection. It has already been anatomy and growth of mildewed barley plants noted that nutrient uptake, photoassimilate would have an effect on root physiology. In the distribution and the balance between growth work carried out by Walters (1981), it was regulators were all altered following infection. shown that roots of mildewed barley were taking up more ³²P-labelled phosphate than Walters (1985) suggested that, powdery uninfected plants by 24 hours after inoculation. mildew infected barley plants might be able to He suggested that this increase was due maintain a functional equilibrium between root primarily to the creation of a sink in the shoot and shoot growth during the early stages of system created by the mildew infection and infection, but that the equilibrium may become secondly to ammonium ions, which were found, increasingly unstable as the pathogen to accumulate in roots of infected plants. It colonises the majority of the plant’s leaf area was also noticed that mildewed plants and the host’s physiology becomes absorbed more potassium and chloride from increasingly altered. the growth medium than healthy plants, and In contrast to the findings on the effects consequently, the ionic content of the tissues of powdery mildew infection in cereals, some of infected plants was greater than those of wild plants have been observed to have their uninfected plants (Walters, 1981). In contrast, roots and shoots more or less equally affected infection by powdery mildew was found to by infection e.g. infection by B. graminis f.sp. decrease nitrate uptake thereby lowering the avenae had no effect on the root to shoot ratio nitrate content of roots and this was explained in a wild oat line compared to the cultivated by the lack of photassimilates received by the oats (Sabri et al ., 1995). Erysiphe fischeri had roots from infected leaves (Walters and Ayres, also no effect on the root to shoot ratio in 1980). However, sodium uptake and content Senecio vulgaris (groundsel) (Ben-Kalio et al ., was unaffected by infection (Walters, 1981). 1979). A similar result was reported for willow- Walters (1981) did suggest that the increased herb infected with the powdery mildew, levels of indole-acetic acid (Shaw et al. , 1958) Sphaerotheca epilobii (Clarke, 1988). The and cytokinin (Vizárová and Minar čic, 1974) failure of powdery mildew infection to alter root found in infected plants could cause increases to shoot ratios in wild oat, groundsel and in the movement of inorganic and organic willow-herb was explained by the ability of nutrients to sites of mildew infection. these hosts to tolerate infection. Other physiological processes in the roots were found to be altered by infection, 4. The effects of infection on host e.g. respiration which increased in the roots of metabolism barley plants whose shoots were infected by mildew (Fric, 1975, Walters, 1981). Invasion of plants by parasitic micro- organisms alters the metabolism of the host in

ISSN: 12895-2007 http://www.egypts e b . o r g Akhkha A., Barley Powdery Mildew ( Blumeria Graminis F.Sp. Hordei): Interaction, Resistance … 7 various ways. Infections by necrotrophic fungi examining the effects of B. graminis f.sp. are generally associated with extensive hordei on the susceptible cultivar Golden damage and the rapid death of affected Promise also found that infection decreased tissues, but relatively simple changes in the rate of photosynthesis from a very early metabolism (Manners, 1993). In contrast, stage of infection. A biphasic inhibition of biotrophic fungi obtain their nutrients from photosynthesis was observed by Edwards living cells and appear to be able to (1970) in barley leaves infected with B. manipulate their host’s metabolism to a graminis f.sp. hordei . The first phase occurred significant extent in order to ensure a within 24 hours after inoculation and the continued supply of carbohydrates and second phase occurred six days after nutrients (Ayres et al ., 1996). inoculation when fungus sporulation on the leaf Biotrophic fungi certainly alter most of had reached its maximum. the physiological and biochemical processes of In the case of oat plants, the effect of their host, including photosynthesis (Buchanan infection was delayed in comparison with et al ., 1981, Ahmad et al ., 1983, Scholes et al ., barley. Haigh et al . (1991) reported that 1985, Scholes, 1992, Ayres et al ., 1996), photosynthesis did not decline in leaves of oat respiration (Last, 1963, Daly, 1976, Raggi, plants infected with B. graminis f.sp. avenae 1980, Kosuge et al ., 1981), carbohydrate until five days after inoculation. Similarly, Sabri metabolism (Whipps et al ., 1981, Farrar, 1985, et al . (1997) observed that the rates of Scholes, 1992, Ayres et al ., 1996), transport maximum gross and net photosynthesis systems (Farrar, 1984), water relations following infection by B. graminis f.sp. avenae (Duniway et al ., 1971b, Ayres 1981a), nucleic decreased eight days after inoculation in one acid metabolism (Chakravorty and Scott, cultivar, but not until ten days after inoculation 1982, Higgins et al ., 1985) and protein in another (Sabri et al., 1997). synthesis (Manners and Scott, 1984). Since Working with pea ( Pisum sativum ) plants this project deals with the effects of B. infected with Erysiphe pisi , Ayres (1976) graminis f.sp. hordei infection on showed that the rate of photosynthesis photosynthesis and respiration in barley, this reduced rapidly from 24 hours of inoculation review will concentrate mainly on these two and had decreased to less than one third of processes and only refer to effects on other that in uninfected plants by the seventh day systems where they impinge on these after inoculation. Similar reductions have been processes. Furthermore, because of the observed in powdery mildew-infected Erysiphe extensive literature on biotrophic parasites, polygoni DC sugar beet leaves Beta vulgaris L only the effects of powdery mildews and rusts (Magyarosy et al ., 1976). will be considered in detail in this introduction. Rust fungi have been reported to have the same effects on photosynthesis as 4.1. Effects on carbon gain through powdery mildew fungi. Wheat leaves infected photosynthesis with Puccinia graminis f.sp. tritici were shown 4.1.1. Effects on photosynthesis in infected to have a reduced rate of photosynthesis leaves together with reduced chlorophyll content from the third day after inoculation (Mitchell, 1979). Since photosynthesis is the process by Barley plants infected with the brown rust which green plants obtain their energy, any fungus, P. hordei , at the first leaf stage pathogen interference with this process will showed no reduction in photosynthesis until clearly have adverse effects on the plant, nine days after inoculation after which the rate leading to decreased growth and yield. of photosynthesis declined to about half that of Powdery mildew and rust infections have the uninfected leaf (Owera et al ., 1981). generally been found to reduce the rates of Scholes et al . (1985) reported that the photosynthesis in their host (Allen, 1942, Daly, reduction in the rate of photosynthesis, both 1976, Magyarosy et al ., 1976, Habeshaw, 1979 per unit leaf area and per unit of chlorophyll, & 1984, Mitchell, 1979, Ellis et al ., 1981, and the changes in vivo chlorophyll Owera et al ., 1981, Gordon et al ., 1982a & fluorescence kinetics clearly indicated that 1982b, Ahmad et al ., 1983). photosynthesis was being progressively In the case of powdery mildews, Allen inhibited within developing pustules of (1942) reported that the rate of photosynthesis Uromyces muscari on bluebell leaves declined rapidly in wheat leaves heavily [Hyacinthoides non-scripta (L.) Chouard ex infected with B. graminis f.sp. tritici , but in Rothm.]. lightly infected leaves the rate of It appears that results even for the same photosynthesis still declined but more slowly. species are contradictory both concerning the Similarly, when barley leaves were infected time and the rate at which changes in with B. graminis f.sp. hordei , the rate of photosynthesis occur following infection. Some photosynthesis began to decline progressively of these differences could be due to the use of from two days after inoculation according to different cultivars with varying degrees of Scott and Smillie (1966), but not until four days susceptibility and which differed in their level after inoculation according to Last (1963) and of tolerance of infection. Hibberd et al . (1996). Habeshaw (1979)

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The reductions in photosynthesis, this case. caused by biotrophic fungi, are sometimes It is widely recognised that infection by preceded by an increased rate during the very fungal biotrophs causes a reduction in early stages of infection particularly when high chlorophyll content although some evidence is concentrations of CO 2 were used (Scott and contradictory. The rate of photosynthesis Smillie, 1966). This effect of high CO 2 expressed per unit of chlorophyll was reported concentration was shown for bean leaves to decrease in barley leaves infected with B. infected by Uromyces phaseoli (Livne, 1964), graminis f.sp. hordei (Allen, 1942). Scott and wheat leaves infected by Puccinia striiformis Smillie (1963) reported a similar effect in (Doodson et al ., 1965), wheat leaves infected barley, but after recalculation of their data, by B. graminis f.sp. tritici (Allen, 1942) and Waygood et al . (1974) found that net barley leaves infected by B. gramins f.sp. photosynthesis per milligram of chlorophyll was hordei (Scott and Smillie, 1966). Studies on actually 50% higher in infected than in barley leaves infected with B. graminis f.sp. uninfected leaves. hordei by Edwards (1970), using ambient CO 2 Other researchers (Paulech et al ., 1970) concentration, observed no initial stimulation found that total chlorophyll was reduced by B. but instead a biphasic inhibition. However, graminis f.sp. hordei in barley leaves before when a high concentration of CO (1%) was 2 photosynthesis had begun to decline. In used stimulation was observed. This contrast, in oak ( Quercus robur L.) leaves stimulation in photosynthesis was attributed to infected with the powdery mildew impairment in glycollate metabolism in infected (Microsphaera alphitoides ), total chlorophyll leaves especially at high CO concentrations. 2 content only began to reduce after 4.1.2. Causes of changes in photosynthesis photosynthesis had begun to decline and A variety of mechanisms have been changes in the chlorophyll a : b ratio were not considered to be responsible for the decrease found until six days after inoculation (Hewitt, observed in photosynthesis following infection. 1976). Photosynthesis can be described as a diffusion Even more contradictory results have process where the flux of CO 2 into leaf is been reported in the case of rust fungal driven by the concentration gradient between infections. For example, in Vigna sesquipedalis the atmosphere and the carboxylation sites. infected by Uromyces appendiculatus , the Models of this diffusion pathway have been reduction in photosynthesis was significantly applied to the analysis of photosynthesis in correlated with the reduction in chlorophyll several host-pathogen systems (Duniway and content between 0 and 14 days after Slater, 1971, Hall and Loomis, 1972, Gordon inoculation (So and Thrower, 1976). Similarly, and Duniway, 1982a). For example, in powdery in wheat infected with stem rust ( P. graminis mildew infection, stomatal resistance was f.sp. tritici ), the decline in the rate of increased by infection, but this change was not photosynthesis per unit of chlorophyll was apparent until three days after inoculation in directly correlated with chlorophyll loss, barley (Ayres, 1979), four days after suggesting that loss of chlorophyll was a major inoculation in pea (Ayres, 1976) and six days contributory factor to the reduction in after inoculation in oak (Hewitt and Ayres, photosynthesis (Mitchell, 1979). 1975). In powdery mildew-infected sugar beet In contrast, no correlation was observed leaves, the decline in net photosynthesis was between the reduction in photosynthesis and attributed not to increased stomatal resistance the reduction in chlorophyll levels in wheat but mainly to increases in mesophyll resistance infected by P. striiformis (Doodson et al ., to CO (Gordon and Dunway, 1982a). 2 1964). Owera et al . (1981) also observed that Similarly, in barley infected with Puccinia although chlorophyll content was depressed in hordei , diffusion of CO into the leaf was found 2 barley leaves infected with P. hordei , both net not to be an important limiting factor in and gross photosynthesis, when expressed per photosynthesis. The main effect of infection, in unit green leaf area, or per chlorophyll content, this case, was to increase CO concentrations 2 increased slightly. This is in agreement with in the intercellular spaces and to double the findings by Last (1963) on the effects of B. mesophyll resistance (Owera et al ., 1981). graminis f.sp. hordei on photosynthesis in In certain infections, particularly those barley leaves. caused by powdery mildew, the decrease Results from studies on the effects of observed in the rate of photosynthesis has downy mildews on photosynthesis in their been partly attributed to a reduction in the hosts are also contradictory. In lettuce infected amount of irradiance reaching the chloroplasts by Bremia lactucae , chlorophyll levels were due to the shading effect of the fungal found to be significantly reduced by six days mycelium present over the surface of the leaf after inoculation (Mason, 1973), but in (Misaghi, 1982). However, in powdery mildew cabbage infected with Peronospora parasitica , of apples, removal of the mycelium did not no chlorophyll loss was observed up to seven lead to any increase in the rate of days following inoculation although chlorophyll photosynthesis and so a reduction in light content may have been altered in the later reaching the chloroplasts was not a factor in stages of infection.

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However, although reducing chlorophyll Wright, 1992). Furthermore, in barley leaves content is one of the features of powdery infected with P. hordei (Ahmad et al ., mildew infections of crop plants, it was not 1982&1984) and in wheat leaves infected with shown by some wild plants in response to P. graminis tritici (Bennet and Scott, 1971), Pi infection; no loss of chlorophyll following was found to have at least doubled in infection was found in the case of willow-herb, concentration compared to uninfected leaves. couch grass or groundsel (Clarke, 1988). Additionally, when Pi was fed to rusted leaves Other evidence suggests that changes in of barley (Scholes and Farrar, 1986) and to the enzyme activities of the chloroplasts and of mildewed wheat (Zulu et al ., 1991), the rate of alterations to chloroplast structure may play a photosynthesis did not increase. Other role in the decline of photosynthesis. Powdery examples have been discussed by Scholes mildew infection of sugar beet was found to (1992), who concluded that Pi is not the result in a substantial reduction in the activity primary factor responsible for the decline in of ribulose-1,5-bisphosphate carboxylase photosynthesis following infection. (RuBPcase), a key enzyme in the reductive Studies of the effects of biotrophic pentose phosphate pathway (Gordon and pathogens on the photochemical reactions of Dunway, 1982b). This decrease was attributed photosynthesis are limited and there is little to a reduction in the concentration of agreement as to their effects. Montalbini et al . RuBPcase as there was no apparent change in (1974) and Magyarosy et al . (1976) reported the specific activity of this enzyme in infected that infection of broad bean leaves by tissue. Similar effects were observed in Uromyces fabae and sugar beet leaves barley leaves infected with powdery mildew infected by Erysiphe polygoni led to a (Walters and Ayres, 1984). Following infection, preferential inhibition of non-cyclic there was a progressive reduction in host photophosphorylation (non-cyclic electron mRNAs encoding both large and small subunits transport chain) as measured in isolated of RuBPcase. Stem rusts have also been chloroplasts. Magyarosy and Malkin (1978) reported to reduce the activity of RuBPcase in investigated the effects of E. polygoni infection wheat (Wrigley and Webster, 1966). on sugar beet further and found that the Reductions in the amount of RuBPcase cytochrome content of the electron transport were reported to be caused by reductions in chain was reduced by 33% in comparison to plant nitrogen in barley infected with B. the controls. This would suggest that infection graminis f.sp. hordei (Walters and Ayres, 1980) by biotrophic pathogens specifically alters the and in barley infected with P. hordei (Ahmad et content of certain carriers involved in electron al ., 1982). The pathogen may also affect the transport, and consequently reduces the rate retranslocation of nitrogen out of infected of non-cyclic electron transport. This view leaves (e.g. Ahmad et al ., 1983). however is not supported by the work of Wynn (1963) using chloroplasts isolated from rust- Gordon and Duniway (1982b) have infected oat leaves, or of Ahmad et al . (1983) suggested that changes in RuBPcase activity using barley leaves infected with brown rust, or may not be entirely responsible for limiting of Holloway et al . (1992) using chloroplasts carbon flux through the reductive pentose from mildewed-barley leaves. All these authors phosphate cycle (RPPC) in mildewed barley, observed no reduction in non-cyclic electron since the activities of RPPC enzymes may also transport. be reduced by infection. Walters and Ayres (1984) in fact noted that the activities of some Recently, Scholes (1992) reviewed enzymes of the pathway were reduced by possible mechanisms responsible for the mildew infection of barley leaves e.g. 3- reduced photosynthesis in infected plants and phosphoglycerate kinase and NADP– suggested that the enzyme invertase could glyceraldehyde phosphate dehydrogenase play a central and linked role in both reducing (GAPDH). photosynthesis and in retaining photoassimilates within infected tissues (see A further explanation for the decline in section 1.5). Increased invertase activity in photosynthesis could be fungal sequestration powdery mildew infected barley leaves resulted of inorganic phosphate (Pi) from the host in the accumulation of sucrose, glucose and tissues. Whipps and Lewis (1981) suggested fructose, causing down-regulation of the Calvin that fungal infection of the leaf induces Pi- cycle by end-product inhibition and by a direct deficiency since biotrophic pathogens act as a effect on genes encoding photosynthetic sink for Pi. Thus the fungus could reduce the enzymes (Scholes, 1992). concentration of host cytosolic and thus chloroplastic Pi, causing a reduction in the rate These contradictory results concerning of photosynthesis. On the other hand, other the effect of infection on photosynthesis and investigations do not support this work. For the mechanisms responsible could well be example, in powdery mildew-infected barley explained by the fact that the different cultivars and wheat leaves the Pi content of the leaf were used of the species investigated. was either unaffected or slightly increased by the time of fungal sporulation (Walters and Ayres, 1981b, Zulu et al ., 1991, Scholes, 1992,

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4.2. Compensatory photosynthesis in energy demand for growth. Furthermore, the uninfected parts of infected plants host, in addition to normal activities, will have The reductions in the rates of a demand to support defence reactions. Such photosynthesis described above have been increases in dark respiration would provide measured in the infected leaves. It is always both energy [NAD(P)H and ATP] and the possible that uninfected tissues of that leaf or carbon skeletons needed for the necessary the uninfected leaves may develop increased biosynthesis (Farrar and Rayns,1987). rates of photosynthesis to compensate for the One of the earliest reports of increased losses from the infected tissues. In this way dark respiration in response to infection is that infected plants may provide sufficient of Yarwood (1934) who showed that infection photosynthates to satisfy all or most sinks at of clover by powdery mildew ( Erysiphe least for some time following infection. polygoni ) increased dark respiration up to 50% Williams and Ayres (1981) demonstrated above the levels of the controls. Working with that net photosynthesis was stimulated in the wheat infected with B. graminis f.sp. tritici , uninfected third leaf of barley plants whose Allen and Goddard (1938) showed that infected lower two leaves were heavily infected by B. leaves respired four-to five-fold more than graminis f.sp. hordei . This stimulation was equivalent uninfected leaves. Other authors greater in water-stressed than in well-watered have confirmed these results for barley plants. Similarly, infections by Erysiphe pisi on infected with B. graminis f.sp. hordei (Millerd the lower three leaves of pea ( Pisum sativum and Scott, 1956, Bushnell and Allen, 1962, L.) stimulated photosynthesis in the uninfected Scott, 1965). Increased respiration has also fourth leaf (Ayres, 1981b). been reported in oak leaves infected with Microsphaera alphitoides (Hewitt and Ayres, Different mechanisms have been 1975). suggested to explain stimulated photosynthesis in the uninfected leaves of infected plants. With powdery mildew infections, it is Walters and Ayres (1983) suggested that this possible to wipe the surface fungal mycelium stimulation in the uninfected upper leaves of from the surface of the leaf leaving only the mildewed barley plants could be due, in part, haustoria in the epidermal cells. The leaf, plus to a transient increase in the content and haustoria have been found to respire at a rate activity of RuBPcase in these leaves. little short of that occurring before removing Increases in the activities of phosphoenol the superficial mycelium, and so most of the pyruvate (PEP) carboxylase and NADP malic increased respiration can be attributed to the enzyme were also observed in this study. host (Daly, 1976). Furthermore, protoplasts isolated from barley leaves infected with B. Walters (1985) suggested that changes graminis f.sp. hordei were found to respire in the nitrate: ammonium balance in infected faster than those from uninfected leaves shoots may also affect the activity of (McAinsh et al ., 1989). RuBPcase. Furthermore, an increased uptake of ³²P-labelled phosphate in barley could Dark respiration was also found to stimulate net photosynthesis, either by increase in hosts infected with rusts. The rate increasing RuBPcase activity or by affecting of dark respiration in whole barley leaves the ratio of ATP: ADP. infected with P. hordei at the time of sporulation was found to be at least twice that Williams and Ayres (1981) suggested of uninfected tissues (Scholes, 1985). Similar that this stimulated photosynthetic activity in values were reported for wheat leaves infected uninfected leaves may allow the plant to with P. graminis tritici (Shaw and Samborski, compensate for the reductions in 1957, Mitchell, 1979), for wheat leaves photosynthesis in infected tissues and for the infected with P. recondita tritici (Staples, 1957) loss of photoassimilates due to the pathogen and for barley leaves infected with P. hordei acting as a sink. Such compensatory activity (Owera et al ., 1981). could well serve to protect the yield of lightly infected plants (Ayres and Zadoks, 1979). The rate of dark respiration is also substantially higher within individual pustules 4.3. Effects on carbon loss through dark of rusts on many hosts than in surrounding respiration uninfected tissues. For example, within 4.3.1. Changes in dark respiration pustules of P. hordei on leaves of barley Another universal effect of biotrophic (Scholes, 1985, Scholes, Farrar, 1986), of fungi is an increase in the rate of dark Uromyces muscari on leaves of bluebell respiration (Daly, 1976, Farrar and Lewis, (Scholes and Farrar, 1985) and of Puccinia allii 1987). Increased dark respiration in diseased on leaves of leek (Roberts and Walters, 1988). plants means that as infection progresses, an These findings lead researchers to hypothesise increasing proportion of newly fixed that in contrast to mildew infections, most of assimilates is lost via respiratory processes the increase in respiratory activity in rusted (Walters, 1985). tissues is contributed by the fungus (Raggi, An increase in dark respiration in 1980, Owera et al ., 1981). However, it is not infected plants may be expected, because in possible to test this hypothesis, since addition to the host, the fungus will have an separating rust fungal tissue from host tissues

ISSN: 12895-2007 http://www.egypts e b . o r g Akhkha A., Barley Powdery Mildew ( Blumeria Graminis F.Sp. Hordei): Interaction, Resistance … 11 is not yet possible. However, since the following chloroplast breakdown, the latter was uninfected regions in wheat around P. graminis observed by Dyer and Scott (1972). tritici pustules (Bushnell, 1970) and in barley Chakravorty and Scott (1982) suggested around P. hordei pustules (Scholes, 1985, that the decline in photosynthesis in rusted Scholes, Farrar, 1986) also show increased and mildewed leaves could also lead to respiration, the host is clearly contributing to increased respiration, since it could lead to the the overall increase in respiration. Respiration release of control mechanisms on glucose-6-P was found to increase in the regions between dehydrogenase and 6-phosphogluconate pustules at both flecking and sporulation dehydrogenase and consequently an increased stages, but was negligible in these regions at activity of the pathway. However, as well as the green island stage (Scholes, 1985). increases in the pentose phosphate pathway, 4.3. 2. Causes of changes in respiratory Daly (1976) suggested that in the later stages rates of infection there may be some uncoupling of Different mechanisms have been oxidative phosphorylation. proposed to explain the rise in dark respiration In the investigation carried out by Farrar following infection. Allen and Goddard (1938) and Rayns (1987) on barley infected with suggested that the increased dark respiration powdery mildew, dark respiration was in wheat leaves infected with B. graminis f.sp. increased by about 80% during fungus tritici was due to substances produced by the sporulation. About half of the increase was due fungus, which diffused into the mesophyll. to increased electron flow through the Similarly, the accumulation of metabolites, cytochrome chain and about half through the often in mobile form, in uninfected cells alternative pathway. The latter showed adjacent to the mildew colonies and in the increased engagement following infection but tissues immediately below, led Bushnell and no increase in capacity. The authors suggested Allen (1962) to suggest that the fungus that the increase in activity of the cytochrome produced diffusible toxic substances that path was due to adenylate regulation, but that caused the rise in the rate of respiration. Later, of the alternative pathway was not understood. Allen (1953) suggested that the toxin In conclusion, whatever the mechanism increased dark respiration by uncoupling or mechanisms behind the increased respiration from energy-requiring processes respiratory activity following infection, it results through activities on oxidative phosphorylation. in the loss of photosynthate that would These activities prevented ATP synthesis and otherwise be utilised for plant growth. lead to ADP accumulation and a higher rate of 4.4. Effects on carbon loss through respiration. A high ADP: ATP ratio was in fact photorespiration found by Poszar and Király (1958) in wheat leaves infected with P. graminis f.sp. tritici . 4.4.1. Changes in photorespiration On the other hand, Scott (1972) The effects of plant infections on suggested that the increase could be due to photorespiration have not been widely quantitative changes in the existing pathways investigated and the existing reports are or, alternatively, to qualitative changes in contradictory. Most reports in fact indicate that respiratory pathways. Daly (1976) in fact leaves infected with biotrophic fungi have suggested that the most likely cause of the rise lower rates of photorespiration than equivalent in dark respiration is a shift from the glycolytic uninfected leaves (Daly, 1976, Farrar and pathway to the pentose phosphate pathway Lewis, 1987). For example, reductions were with increased activity of the latter pathway. found in barley leaves infected with B. The involvement of the pentose phosphate graminis f.sp. hordei (Ayres, 1979, Walters and pathway in the rise in rates of respiration is Ayres, 1984) and also in oak leaves infected supported by the finding that the activities of with M. alphitoides (Hewitt and Ayres, 1975). the enzymes of this pathway increased after Similarly, some rust fungi e.g. Melampsora lini infection. Indeed, Scott (1965) reported a two in flax were found to decrease the rate of to three fold increase in the activities of photoresoiration (Akhkha, 2003b). glucose-6-P dehydrogenase and 6- However, in a few cases increases in the phosphogluconate dehydrogenase. rate of photorespiration following infection The pentose phosphate pathway seems have been reported. Thus Ayres (1976) to be located in the cytosol and is limited by observed an increase in pea leaves infected the availability of NADP +. The rise in the with the powdery mildew Erysiphe pisi , while a respiratory activity observed in mildewed similar increase was observed in barley leaves barley leaves may be a direct response to the infected with P. hordei (Owera et al ., 1981). To change in the NADP +: NADPH balance (Scott add to the confusion, Mitchell (1979) found no and Smillie, 1966, Dyer and Scott, 1972). Ryrie differences in rates of photorespiration and Scott (1968) suggested that the enhanced between healthy wheat leaves and leaves activity of the pentose phosphate pathway infected by P. graminis f.sp. tritici . observed in rust and mildew infections could be due to the release of NADP + into the cytosol

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4.4.2. Causes of changes in that assimilates continued to be imported from photorespiration uninfected leaves into infected leaves. Similarly, Livne and Daly, (1966) observed that Walters (1985) reported that reductions 14 in photorespiration in infected plants could be when C-labelled CO 2 was fed to uninfected due to reductions in the activities of associated trifoliate leaves of bean plants the label enzymes. For example, in barley leaves accumulated in primary leaves infected with U. infected with B. graminis f.sp. hordei (Walters appendiculatus . Siddiqui and Manners (1971) and Ayres, 1984) and in oak leaves infected also showed that infection of wheat leaves by Puccinia striiformis increased the amount of with M. alphitoides (Hewitt and Ayres, 1977), 14 the activity of the enzyme glycolate oxidase C-labelled assimilates moving to infected was found to be lower than in uninfected leaves. However, when single leaves of wheat tissues. The activity of this enzyme was were infected with P. striiformis they did not reported to have decreased in wheat leaves attract assimilate movement from other leaves infected with P. graminis tritici (Kiraly and (Doodson et al ., 1965). Farkas, 1957). In addition, Walters and Ayres Inorganic ions have also been shown to (1984) found that the activities of glyoxylate preferentially move to infected parts of the reductase and RuBPoxygenase also decreased plant (Gerwitz et al ., 1965, Yarwood and following infection. However, the mechanism Jacobsen, 1955). For example, Ahmad et al . responsible for the stimulation of (1982) demonstrated that not only photorespiration in barley leaves infected with carbohydrates but also nitrogen, phosphorus P. hordei reported by Owera et al . (1981) has and potassium were retained to a greater not been not understood. extent in barley leaves infected with P. hordei 5. Effects of infection on translocation than in uninfected leaves as the leaves age. The effects of biotrophic pathogens on Conversely, other workers demonstrated the translocation and distribution patterns of a decrease in sugar content of leaves infected assimilate throughout the plant have been by rusts. Thus, Murphy (1936) observed a investigated by many workers (Crowdy and decrease in soluble sugars in oat plants Manners, 1971, Manners and Myers, 1973, infected with Puccinia coronata . Similarly, the Whipps et al ., 1981, Farrar, 1984, Farrar, total sugar content and especially the sucrose 1992). Because an infected leaf typically has a fraction, decreased only slightly in leaves of a lowered rate of photosynthesis, an additional resistant wheat cultivar infected with P. sink for assimilates in the form of the graminis but to a significant extent in a pathogen, and an increased rate of dark susceptible one (Krog et al ., 1961). respiration, less translocation from it would be The reduction of assimilate export from expected. In general, infection by biotrophic infected organs and the increased import of fungi results not only in a reduction in the assimilates to that organ would deprive other export of assimilates from infected leaves organs, such as roots, of required assimilates. (Doodson et al ., 1965), but it also promotes In the case of powdery mildew infections, imports into those tissues (Shaw and reductions in the percentage of assimilate Samborski, 1956, Livne and Daly, 1966). translocated to roots were observed in barley In the case of powdery mildew infections, plants by Edwards (1971) and Fríc (1975) and Fríc (1975) observed that export from the first in wheat by Lupton et al . (1973). Edwards leaves of barley plants infected with B. (1971) attempted an analysis of the fate of graminis f.sp. hordei was less, although export imported assimilates within roots of barley plants infected by B. graminis f.sp. hordei . He from uninfected second leaves was greater, 14 five days after inoculation. found that when CO 2 was fed to the tips of infected leaves, labelling of ethanol-soluble Rust fungi were found to behave in the compounds was reduced much more than that same way as powdery mildews. Thus, Doodson of ethanol-insoluble compounds when import et al . (1965) found that when a single leaf of a was reduced. Fric (1975) observed that when wheat plant was infected with Puccinia barley leaves were infected with B. graminis striiformis , the proportion of the assimilates f.sp. hordei , the absolute amount of labelled exported was only 0.4% compared with 20% assimilate reaching the roots from the infected from a corresponding healthy leaf on an leaves in the 24 hours after feeding was uninfected plant. It has also been shown that reduced by 27% following infection, while the uninfected primary leaves of Phaseolus amount remaining in the shoots was reduced vulgaris fed with 14 C-labelled CO exported 2 by 20%. Walters and Ayres (1982) concluded 50% of the label in a five-hour period, whereas that reduction in the growth of primary roots of primary leaves infected with Uromyces barley infected with B. graminis f.sp. hordei appendiculatus exported less than 2% in a was due to a reduction in the specific activity similar time interval (Livne and Daly, 1966). of different assimilates fractions within the In some cases infection may not only roots (soluble, storage and structural). reduce export of carbohydrates from an organ, Similarly, infection of wheat leaves with B. but also promote import into that organ. For graminis f.sp. tritici , also reduced the example, in oak plants infected with M. percentage of labelled assimilates exported to alphitoides , Hewitt and Ayres (1976) observed

ISSN: 12895-2007 http://www.egypts e b . o r g Akhkha A., Barley Powdery Mildew ( Blumeria Graminis F.Sp. Hordei): Interaction, Resistance … 13 the roots in three susceptible cultivars fed closure 14 CO 2 at the third, fifth or flag leaf stages Infections of barley leaves by (Lupton et al ., 1973). Rhynchosporium secalis (Ayres et al ., 1975) Rust fungi were also reported to reduce and of potato by the blight fungus, the amount of assimilates translocated to Phytophthora infestans (Farrell et al ., 1969) roots. For example, Siddiqui and Manners caused an increase in the rate of transpiration (1971) showed that infection of wheat leaves from the infected area of the leaf both in the by Puccinia striiformis decreased the amount light and in the dark. This increase was of 14 C-labelled assimilates moving to the roots. attributed to an increase in the mean stomatal The magnitude of changes in assimilate aperture in the infected area in the light and translocation in response to biotrophic the failure of the stomata to close in the dark. pathogen attack may depend on many factors, The downy mildew fungus Peronospora including environmental conditions, level of tabacina has also been found to affect infection, level of host resistance and level of stomatal opening in the leaves of its host host tolerance of the parasite. tobacco in a similar manner (Cruickshank and Rider, 1961). From the considerable experimental evidence currently available, several In contrast, stomatal opening in the light mechanisms have been proposed to be has been reported to be inhibited by rust and responsible for the disruption of assimilates powdery mildew infections as well as by some translocation in infected plants. Firstly, viruses such as sugar beet yellows virus (Hall Thrower (1965) attributed the reduced et al ., 1972). translocation from infected leaves to the rest of Transpiration in rust and powdery mildew the plant simply to the direct effect of the infected tissues usually follows the pattern of pathogen providing an active sink for nutrient stomatal behaviour, decreasing in the light and substances. This was experimentally increasing in the dark (Walters, 1985). Rust demonstrated by the work of Edwards et al . fungi enter their hosts through stomatal pores, (1966) who found that carbon transfer from develop mainly in the intercellular spaces of infected barley leaves to B. graminis f.sp. the leaf and inhibit stomatal movements hordei was very rapid. progressively until eventually the stomata In contrast, Whipps and Lewis (1981) became fixed in an almost closed position and Farrar (1984) proposed a number of (Duniway et al ., 1971a). However, with rust combinations of mechanisms, which may be fungi, once fungal sporulation has ruptured the responsible e.g. changes in growth regulator cuticle, non-stomatal transpiration increases concentrations, altered permeability of infected and becomes the significant factor (Johnson et cells, increased activity of invertase and al ., 1934 & 1940, Murphy, 1935). amylase and changes in the concentration of Paul and Ayres (1984) showed that after orthophosphate (Pi). sporulation, groundsel ( Senecio vulgaris ) 6. Effects of infection on water relations leaves infected with Puccinia lagenophorae transpired much more rapidly than did healthy Water plays a very important role in all controls. The same results were shown by physiological processes in plants including Duniway et al . (1971a) in bean ( Phaseolus photosynthesis, respiration, translocation, vulgaris ) leaves infected with Uromyces partitioning of metabolites, stomatal behaviour, phaseolus. protein synthesis, cell division, cell elongation and cell wall synthesis. Water stress will lead Powdery mildew infections result to the perturbation of all or some of these generally in a failure of stomata to open fully in physiological processes and consequently will the light and to close fully in the dark lead to reductions in plant growth and yield (Majernick, 1971, Ayres, 1976). Wheat leaves (Kramer, 1983). infected with B. graminis f.sp. tritici were shown to have a significantly reduced Healthy plants can protect themselves stomatal opening within three to six hours against the development of water stress by after inoculation (Martin et al ., 1975). regulating stomatal aperture. The stomata are Majernick (1965) working with barley leaves sensitive structures that represent the greatest infected with B. graminis f.sp. hordei reported variable resistance in the pathway of water that stomatal transpiration had reduced within movement through the plant (Ayres, 1981a) one day after inoculation. Ayres (1979) also, and any biotic or abiotic factor causing using barley leaves infected with B. graminis changes in the pattern of stomatal behaviour f.sp. hordei , observed that reduced stomatal will affect plant water relations and opening was not apparent until three days after consequently perturb growth and development. inoculation. Other plant species other than Many investigations have been carried out to cereals showed similar responses to mildew determine the effects of obligate biotrophs on infection. For example, although garden pea stomatal behaviour. These effects have been (Pisum sativum ) leaves infected with E. pisi found to differ from one pathogen to another showed an initial increase in stomatal opening and from one host to another. within the first 48 hours of inoculation, the 6.1. Effects on stomatal opening and stomatal opening became progressively

ISSN: 12895-2007 http://www.egypts e b . o r g 14 Egypt. J. Exp. Biol. (Bot.), 5: 1 – 20 (2009) reduced in the light and stomata failed to close cereals (barley and wheat) was attributed to completely in the dark (Ayres, 1976). Thomas the lack of production of volatile substances in et al . (1982) observed a 50% reduction in peas infected with Erysiphe pisi or to the stomatal aperture five days after inoculation in differences in the turgor pressures of guard sugar beet ( Beta vulgaris ) leaves infected with cells and epidermal cells (Ayres, 1976). E. polygoni . Similar responses were observed Furthermore, Ayres (1980) suggested that in leaves of oak plants infected with stomatal opening could be inhibited by Microsphaera alphitoides , but not until six substances synthesised by the host such as days after inoculation, although, transpiration pisatin (a pterocarpan) which accumulates in rates increased within two to three days pea leaves infected with E. pisi . after inoculation (Hewitt et al ., 1975). The increased rate of transpiration 6.2. Causes of changes in stomatal function observed in barley leaves infected with B. Ayres (1972 & 1975) investigated graminis f.sp. hordei when 50% of the leaf was stomatal functioning in barley leaves infected covered by mildew, was attributed to cuticular with Rhynchosporium secalis and suggested injuries caused by the infection (Majernick, that in the early stages of infection the 1965, Paulech et al ., 1970). In contrast, the increase in stomatal aperture was a result of increase in the rate of transpiration observed the loss of osmotically active solutes from the in oak leaves infected with Microsphaera epidermal cells of diseased leaves which alphitoides was attributed mainly to the fungal consequently altered the turgor relations mycelium itself (Hewitt et al ., 1975). between guard cells and their surrounding Many of the differences in host response epidermal cells. The increase in transpiration to different pathogens are most likely to be at later stages of infection was attributed to mainly due to the different ways the pathogens water loss through the ruptured cuticle (Ayres, grow and develop on or within their host’s 1975). tissues. However, the experimental differences In the case of barley infected with B. in host response reported for particular graminis f.sp. hordei , Majernick (1965) pathogens are also likely to be due to an suggested that a volatile product was involved extent to the experimental procedures used, in the inhibition of stomatal opening in the but are also likely to be due to the fact that light. A similar suggestion was made by Martin different cultivars were used. et al . (1975) for wheat leaves infected with B. One significant factor missing from most graminis f.sp. tritici . of the studies was any measure of the way in The increased stomatal opening in the which or the rate at which parasite biomass light that occurs in pea leaves infected with E. accumulated during the course of the pisi 48 hours after inoculation contrasts with experiments. Even when parasite biomass the reduced stomatal opening in wheat within 6 accumulated to similar extents in the different hours of inoculation (Martin et al ., 1975) and in cultivars used, reactions may be different due barley within 24 hours after inoculation to different tolerances of the parasite in the (Majernick, 1965) with the cereal powdery tissues. mildew. The difference between peas and

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