Mutual Benefits Through Formalized International Collaboration on Biological Control of Weeds with Plant Pathogens
Mutual Benefits through Formalized International Collaboration on Biological Control of Weeds with Plant Pathogens
Dana Berner, Foreign Disease-Weed Science Research Unit, Agricultural Research Service, U.S. Department of Agriculture, Ft. Detrick, Frederick, MD 21702, USA, Thouraya Souissi, Institut National Agronomique de Tunisie, 43 Avenue Charles Nicolle, 1082 Tunis-Mahrajène, Université de Carthage, Tunisia, Emily Smallwood, Craig Cavin, Farivar Eskandari, Foreign Disease-Weed Science Research Unit, Agricultural Research Service, U.S. Department of Agriculture, Ft. Detrick, Frederick, MD 21702, USA, Berna Tunali, Phytopathology Division, Department of Plant Protection, Agricultural Faculty, Ondokuz Mayis University, 55139, Kurupelit, Samsun, Turkey, Orhan Buyuk, Aysegul Yildirim, Plant Protection Central Research Institute, P.O. Box 49 06172, Yenimahalle, Ankara, Turkey, Zhanna Mukhina, The All-Russia Rice Research Institute, Krasnodar, Belozerny, 350921, Russia, Tamara Kolomiets, The All-Russia Research Phytopathology Institute,Moscow Region, B. Vazemy, 143050, Russia, Tatiana Matveeva, Denis Bogomaz, The Department of Genetics and Breeding, Saint Petersburg State University, Saint Petersburg, Russia, Damenique Kassanelli, Department of Botany, Kuban State University, Krasnodar, Russia, Dorsaf Mejri, Institut National Agronomique de Tunisie, 43 Avenue Charles Nicolle, 1082 Tunis- Mahrajène, Université de Carthage, Tunisia, Kawther Latiri, Institut National des Recherches en Génie rural, Eau et Forets, B.P 10, 2080 Ariana, Université de Carthage, Tunisia, Javid Kashefi, European Biological Control Laboratory, American Farm School, P.O. Box 23, 551 02, Thessaloniki, Greece, and Anastasia Lagopodi, Aristotle University, Thessaloniki, Greece ______
ABSTRACT Berner, D., Souissi, T., Smallwood, E., Cavin, C., Eskandari, F., Tunali, B., Buyuk, O., Yildirim, A., Mukhina, Z., Kolomiets, T., Matveeva, T., Bogomaz, D., Kassanelli, D., Mejri, D., Latiri, K., Kashefi, J., and Lagopodi, A. 2011. Mutual benefits through formalized international collaboration on biological control of weeds with plant pathogens. Tunisian Journal of Plant Protection 6: 49-74.
In the U.S., introduced invasive weeds have catastrophic effects on agricultural, aquatic, rangeland, riparian, and natural ecosystems. In the latter three ecosystems the only economically feasible means for controlling these weeds is often classical biological control through the introduction of natural enemies, including plant pathogens, from areas where the weed species are native and naturally suppressed. In order to pursue classical biological control of weeds with plant pathogens, the Foreign Disease-Weed Science Research Unit (FDWSRU) of USDA, ARS relies on international collaboration with scientists in countries where the weed species are native. Results of these collaborations are summarized herein to highlight the mutual benefits that can be gained from formal international collaboration on biological control of weeds with plant pathogens. FDWSRU has been successfully
Tunisian Journal of Plant Protection 49 Vol. 6, No. 1, 2011 working on classical biological control of invasive weeds with plant pathogens for over 30 years. However, in order to discover new accessions of weed pathogens, collaboration with scientists in regions where the target weeds are native is essential. Until recently, however, these scientists were not actively involved in biological control of weeds; as such activities were not funded or sanctioned in their countries. Now, due to increasing farmer (and consumer) demands for effective inexpensive and safe weed control, increasing organic agricultural production, increasing restrictions on herbicide use, and increasing herbicide resistance of weeds, inundative biological control and mycoherbicides are becoming an attractive alternative to chemical herbicides and are of increasing interest to many scientists worldwide. This mutual interest in biological control has resulted in several formal and successful collaborative projects over the last 10 years between FDWSRU and international scientists. These projects in Turkey, Tunisia, Greece, and Russia have resulted in discoveries of many new diseases of weeds which, in turn, have led to numerous reports of newly discovered pathogens from these weeds. As reports of new pathogens and their potential appear in the literature, administrators are becoming more aware of the overall potential of this approach and are more willing to support new biological control projects.
Keywords : classical biological control, field testing, international collaboration, inundative biological control, mycoherbicides, pathogens, weeds ______
1. INTRODUCTION The Foreign Disease-Weed Science where many of the invasive weeds in the Research Unit (FDWSRU) of USDA, U.S. are native, interest in biological ARS has been successfully working on weed control is driven not only by local classical biological control of invasive concerns for food safety and effective weeds with plant pathogens for over 30 inexpensive weed control, but also by years (18). However, new weed increasing organic agricultural production pathogens, from regions where the target (76). There are additional concerns about weeds are native, are always needed. The increased restrictions on herbicide use in most effective, legal, and ethical way of Europe and what this might portend discovering and collecting new weed locally. In addition, increasing instances pathogens is through formal collaborative of herbicide resistant weeds (36) are projects with international scientists and leaving fewer alternatives for weed their institutes. Over the last 10 years, control. As a result, formal collaborative interest in biological weed control has projects on biological weed control with gradually increased within the plant pathogens are finding more international scientific community (12), acceptance within these regions, and this arises, in part, from consumer particularly since these projects can concerns on the impact of pesticides on provide some funding that can advance food safety which have been steadily biological control in these countries and increasing since 1989 (20). In the in the U.S. Mediterranean and Eurasian regions, The general objective of such a collaborative project is, usually, to establish long-term collaboration on Corresponding author: Thouraya Souissi collection, evaluation, and Email: [email protected] characterization of pathogens of weeds of
importance to the collaborating country Accepted for publication 19 July 2011 and to the U.S. Typical sub-objectives are: (1) discover diseases of weeds in the Tunisian Journal of Plant Protection 50 Vol. 6, No. 1, 2011 collaborating country from weeds of During the last 10 years FDWSRU importance in both the U.S. and the has developed collaborative projects on collaborating country, (2) jointly isolate biological control of weeds with plant and identify pathogens responsible for pathogens in Turkey, Tunisia, Russia, and these diseases, (3) jointly develop Greece. Some of the results and potential procedures for evaluation and mutual benefits of these projects are characterization, including host range, of discussed. pathogens in the field and in the greenhouse, (4) field test pathogens 2. COLLABORATION WITH collected in the collaborating country on TURKEY weeds of importance to the U.S. and the 2.1. Background. collaborating country, (5) independently, Formal collaboration on biological and through scientific exchange visits, control of weeds with plant pathogens evaluate and characterize pathogens in began in the spring of 2001 between the different environments and share data and senior author at FDWSRU and Dr. B. results, (6) facilitate releases of biological Tunali, a plant pathologist at the Plant control pathogens in the U.S. and Protection Central Research Institute development of mycoherbicides, based on (PPCRI), Ankara, Turkey. This these pathogens, in the collaborating collaboration was initiated through a country. fellowship from the Organization for Any work on exotic pathogens in Economic Co-operation and the U.S. is restricted to quarantine Development (OECD) for the senior laboratory and greenhouse facilities. author to visit PPCRI for six weeks and Collaborative biological control projects establish longer term collaboration on provide the opportunity for field testing biological control of weeds with plant of the pathogens in their native range. pathogens. In 2002, a three-year project Testing for efficacy and host range under between FDWSRU and PPCRI was field conditions can demonstrate what funded by the USDA Foreign risks, if any, are associated with these Agricultural Service to continue pathogens and how any risks could be collaboration initiated by the OECD minimized in both the collaborating fellowship. A weed scientist from PPCRI country and the U.S. Field test sites can was added to the project, along with Dr. also be used for more comprehensive Tunali, as a co-principal investigator. pathogen evaluation by providing After the project terminated, informal opportunities to measure plant damage collaboration has continued, until now, under different field conditions and between FDWSRU and PPCRI. When disease progress under different Dr. Tunali moved to Ondokuz Mayis environmental conditions. Data from University (OMU) in Samsun, Turkey, these tests can help improve pathogen the bulk, but not all, of this informal deployment for both classical and collaboration followed and now continues inundative biological control. If even one predominantly with OMU. A cooperative mycoherbicide is successfully developed agreement between FDWSRU and OMU in a country, collaboration could be self- is pending, but more external funding is sustaining and efficiently lead to more needed to further develop some of the releases of effective biological control potential mycoherbicides in Turkey. agents in the U.S. while also providing direct agricultural and economic benefits locally. Tunisian Journal of Plant Protection 51 Vol. 6, No. 1, 2011
2.2. Weed targets and pathogens treatment of these taxonomically difficult for biological control of weeds in the fungi. Unfortunately, molecular U.S. and Turkey. taxonomy has not provided a solution yet, A total of 654 disease specimens as there are internal transcribed spacer were collected from 30 different genera (ITS) 1, 5.8S ribosomal DNA, and ITS2 and 36 species of weeds from 2001 to (hereafter referred to collectively as ITS) 2010 in Turkey. From these diseases, 83 DNA sequences of 69 isolates of fungi pathogens were isolated and identified at from different hosts named P. exigua or least to genus. Of these pathogens, eight the synonym Boeremia exigua in were judged to be promising potential GenBank. These sequences all align with biocontrol agents for weeds in the U.S. each other. The host range of the fungus (classical biological control) and/or is currently being evaluated in quarantine Turkey (inundative biological control). at FDWSRU, and significant damage Descriptions of the target weeds and the attributable to disease caused by the status of development of these promising fungus has only been found on the target, potential control agents follow. out of 51 related plant species evaluated thus far. Given the high degree of host 2.2.1. Russian knapweed (RK) specificity, this isolate should probably (Rhaponticum repens (L.) Hidalgo, better be named P. exgiua var. acroptili Asteraceae). Rhaponticum repens but doing so only further complicates the =Acroptilon repens (L.) DC.; Russian tangled taxonomic problems by naming knapweed; synonym Centaurea repens yet another variety of this fungus. The L., Asteraceae) is an introduced perennial fungus causes necrosis of the leaves and invasive weed in the U.S. present in 27 once symptoms progress to the mid-veins states and declared a noxious weed in 18 of the leaves, the disease progresses states (71). It is also becoming a noxious rapidly, indicating the possibility of weed in wheat fields in Turkey (40, 65, systemic infection or systemic movement 66). It is a target of biological control of toxins. Diseased plants usually die efforts in both countries. More within two weeks of inoculation. Severe information on this weed can be found in disease can be produced by inoculation of the element stewardship abstract by foliage with an aqueous suspension of Carpenter and Murray (21). conidia. These characteristics make this isolate of PEE a potential candidate for 2.2.1.1. Phoma exigua var. exigua biological control of this weed in Turkey. Desmaz. Tunali et al . (69) reported that in A voucher specimen has been deposited the summer of 2002, they had found with the U.S. National Fungus dying RK plants on a roadside near Collections (BPI 843350) and ITS Cankiri, Turkey. The fungus responsible sequences were deposited in GenBank for the disease was isolated and identified (accession #AY367351). as Phoma exigua var. exigua (PEE) In 2004 field inoculations of RK Desmaz (69). However, there are many with PEE were done in Ayas, Turkey. strains of P. exigua and over 300 Inoculated plants were sprayed with synonyms, including varieties and special aqueous suspensions of spores at a forms, of this fungus associated with concentration of about 10 6 spores/ml. In nearly 700 host plants (33). This Ayas, the pathogen established quickly in variability reflects the observed host- 2004, and there was 100% incidence on specificity of many of the varieties and inoculated plants by four months after special forms and the poor taxonomic inoculation (Fig. 1). Tunisian Journal of Plant Protection 52 Vol. 6, No. 1, 2011
Fig. 1. Symptoms caused by Phoma exigua var. exigua on Russian knapweed in the field in Turkey.
Disease severity (percent of 2.2.1.2. Cercosporella acroptili diseased leaf tissue) was about 50%. (Bremer) U. Braun. In 1998, a There were no RK plants found in this widespread foliar disease of RK was field in 2005. In 2005, field plots were found near Isparta, Turkey (11). In 2001, inoculated in Polatli, Turkey. Disease the disease was found again at the same established more slowly in Polatli than in site, and Cercosporella acroptili Ayas, possibly because of an extended (Bremer) U. Braun was isolated from the dry period following inoculation. diseased tissue. A specimen was However, in the spring of 2006, the deposited in the U.S. National Fungus disease was widespread in Polatli and the Collection (BPI No. 871029) and ITS amount of RK was about 2/3 of that prior sequences were deposited in GenBank to inoculation. In 2010, plants of RK (accession # AY961597.1). At the time, it were inoculated in the field at Ayas, and was thought that this fungus had potential disease progress data, in relation to as both a classical biological control environmental variables, is being agent in the U.S. and an inundative agent collected. More field research is in Turkey. However, the fungus has since necessary to determine optimum been found in the U.S (31) and does not inoculation times and spread of the seem to cause extensive damage to RK in pathogen in space and time. This isolate this country. It may be possible to of PEE grows well on both solid and augment PEE mycoherbicide liquid artificial media and is thus formulations in Turkey with C. acroptili amenable to mass production in aerobic spores to heighten efficacy on RK . Both conditions. Spore production in both single and mixed formulations of C. types of media is high, and development acroptili should be developed and tested of oil formulations, containing at least 10 6 as potential mycoherbicide components. spores/ml, should not be a problem.
Tunisian Journal of Plant Protection 53 Vol. 6, No. 1, 2011
2.2.1.3. Puccinia acroptili Syd. & P. (16), and no disease severity differences Syd. In 2002, an aggressive and were found among N. American, Turkish, damaging rust was found on RK along and Russian isolates. As introduction of the Ankara to Cankiri road in Turkey. the Turkish isolate into the U.S. would The rust was as attributed to Puccinia provide no additional biological control, acroptili and, although this rust was further work on this rust ceased. A known to exist in North America (61), it specimen has been deposited in the U.S. was thought that this isolate might be National Fungus Collection (BPI 877990) significantly more aggressive and and ITS sequences were deposited in damaging (Fig. 2) than North American GenBank (accession # HQ700340). isolates. This turned out not to be the case
Fig. 2. Rust pustules of Puccinia acroptili on the leaves of Russian knapweed in a quarantine greenhouse in the U.S.
2.2.2. Medusahead ( Taeniatherum florets (ovaries) of medusahead plants in caput-medusae subsp. asperum (L.) a weedy field between Sabanozu and Nevski, Poaceae). Medusahead is a Gumerdigin, Turkey. The smut was winter annual grass native to the identified morphologically as Ustilago Mediterranean and Eurasian regions (49), phrygica (72). This smut fungus was but it is an extremely invasive weed in the intriguing because it is an obligate plant southwestern U.S. (78). It is present in 10 pathogen that was thought to likely be U.S. states and declared noxious in five very host specific. Infection of (71). It is a target of biological control medusahead plants with the fungus efforts in the U.S. It is widespread on the results in partial systemic disease in Anatolia Plateau in Turkey but is not which some tillers and florets are considered an agricultural problem there. diseased while others on the same plant remain healthy (Fig. 3). Ustilago phrygica Magnus. In 2001 a smut fungus was found in the
Tunisian Journal of Plant Protection 54 Vol. 6, No. 1, 2011
Fig. 3. Spikes of medusahead plants smutted by Ustilago phrygica. (A) Smutted spike with typical peridium, (B) Diseased spikes with systemic disease (leftmost) and typical partial systemic disease (rightmost). The healthy spike in the lower right background (arrow) is from a tiller on the same plant as the diseased spikes.
Diseased florets only produce smut Desv. HC is a native perennial plant in teliospores while disease-free florets on North Africa, temperate Asia, and Europe infected plants produce seeds normally. (47, 70) and is an introduced invasive However, after host-range determination weed in the U.S. that is present in 39 tests at FDWSRU, slender wheatgrass states and declared noxious in 15 states (Elymus trachycaulus subsp. (71). It is a member of the Brassicaceae trachycaulus ), a native North American family that includes many cultivated, forage grass, was found susceptible to the introduced crops and native plants in the smut (7). This corresponded to U.S. (39). Because of the large number of observations of Nielsen (55). This non- related species in the U.S., HC is a target effect, and the likelihood of others, difficult classical biological control target in combination with the relatively minor that will require a very host-specific and, damage i.e. partial disease caused us to simultaneously, aggressive pathogen. The abandon further work with the fungus. A weed is not a problem in Turkish sample of the smut was deposited in the agriculture. U.S. National Fungus Collections, BPI 871725, and the ITS sequence was Septoria lepidii Desm. In 2001, an deposited in GenBank (accession # epidemic of diseased and dying HC plants DQ139961). was found along the Haymana to Polatli Road in Turkey. Diseased leaves of these 2.2.3. Hoary cress (HC) ( Lepidium plants were covered with pycnidia of a draba L., Brassicaceae). Synonyms of fungus (Fig. 4), and severely diseased Lepidium draba include L. draba (L.) plants were defoliated. subsp. draba and Cardaria draba (L.)
Tunisian Journal of Plant Protection 55 Vol. 6, No. 1, 2011
Fig. 4. Leaves of Lepidium draba covered with pycnidia of Septoria lepidii.
Diseased leaves were taken to the with some difficulty, be manipulated to laboratory at PPCRI and placed in moist sporulate but it behaves nearly as an chambers. Within two days, most of the obligate plant pathogen. If the authors can pycnidia oozed masses of filiform and succeed in reliably reproducing the septate spores typical of the genus disease caused by the fungus, then the Septoria. Measurements of the spores and expectation is that this fungus would be pycnidia characteristics conformed to the very host-specific and aggressive enough description of Septoria lepidii Desm. (3). to be a promising biological control agent Since 2001, this leaf spot disease, of HC. The fungus has only been reported putatively caused by S. lepidii, has been on Cardaria and Lepidium spp. (33) that found by the authors in many other are not native to the U.S. (39). locations in Turkey, Tunisia, Greece, and Russia, and it seems that the disease is 2.2.4. Bindweeds (BW) widely distributed in the native range of (Convolvulus arvensis L. and Calystegia the weed and likely contributes to natural sepium (L.) R. Br., Convolvulaceae). control of the weed. However, despite Field and hedge bindweeds ( Convolvulus numerous attempts, the authors have not arvensis and C. sepium , respectively) are been able to complete the proofs of virtually cosmopolitan in their world- pathogenicity (Koch’s postulates) of this wide distribution (48, 70) and are among fungus on HC. Although the disease has the worst weeds in the world (37). These been found in many locations and S. weeds have been targets for inundative lepidii consistently isolated from diseased biological control with plant pathogens as leaves in each location, it is not possible part of the European COST Action 816 to conclusively state that the disease is project (26). Research under this project caused by S. lepidii without fulfilling resulted in the successful development of Koch’s postulates (1). Moreover, without an isolate of the fungus Stagonospora being able to reliably reproduce the convolvuli Dearn. & House as a potential disease, it is not possible to conduct any mycoherbicide component (58) for efficacy or host-range testing of the control of both bindweeds. Although this fungus. In artificial culture medium, this fungus successfully controls the is a very slow-growing fungus that can, bindweeds, a commercial mycoherbicide Tunisian Journal of Plant Protection 56 Vol. 6, No. 1, 2011 based on the fungus has yet to be background work should facilitate developed, apparently due to lack of development of a bindweed commercial interest in Europe (M.O. mycoherbicide with the isolate of S. Ahonsi, personal communication). In convolvuli found in Turkey (Fig. 5a). Turkey, however, there is commercial The other fungus that has been interest in a bindweed mycoherbicide (46, extensively evaluated is P. convolvuli . 68), but development of a suitably This fungus was discovered on C. aggressive and specific pathogen remains arvensis and newly described in 1988 to be done. (56, 57). In 1993, the use of the fungus as 2.2.4.1. Stagonospora convolvuli a biological control agent for C. arvensis Dearn. & House; Phomopsis convolvuli was patented (74). The discovery of this Ormeno-Nuñez, Reeleder & A.K. pathogen in Turkey (46, Fig. 5b) was Watson; and Colletotrichum cf. linicola only the second report of this pathogen of Pethybr. & Laff. C. arvensis in the world. These three fungi were collected and Although no commercial isolated from C. arvensis in Turkey from mycoherbicide was developed from the 2001 to 2010. Two of the three species fungus in North America, possibilities have been evaluated elsewhere and been exist in Turkey to use the fungus alone or shown to be promising biological control in combination with S. convolvuli and/or fungi. The isolate of S. convolvuli that C. linicola as a multicomponent was developed in Europe has been mycoherbicide. These combinations are thoroughly tested and found safe to use as beginning to be field tested. a mycoherbicide component (15). This
Fig. 5. Symptoms caused by Stagonospora lepidii on Convolvulus arvensis (A), Phomopsis convolvuli on Convolvulus arvensis (B), and Colletotrichum cf. linicola on Convolvulus arvensis leaves (C).
Tunisian Journal of Plant Protection 57 Vol. 6, No. 1, 2011
The discovery of Colletotrichum cf. and 19 species of weeds from 2001 to linicola in Turkey as a pathogen of C. 2010 in Tunisia. From these diseases, 19 arvensis (68, Fig. 5c) is the only report in pathogens were isolated and identified at the world of a Colletotrichum sp. least to genus. Of these pathogens, two, parasitizing C. arvensis (33). Of the 100 that had not been isolated elsewhere, mycoherbicide projects listed by were judged to be promising potential Charudattan in 1991 (23), eighteen of biological control agents for weeds in the these involved a Colletotrichum sp., and U.S. (classical biological control) and/or this pathogen genus has a long successful Tunisia (inundative biological control). history as a mycoherbicide component Descriptions of the target weeds and the (25, 53). To determine whether this status of development of these promising Colletotrichum species has potential as a potential control agents follow. mycoherbicide component for C. arvensis and C. sepium control in Turkey, 3.2.1. Hoary cress (HC) ( Lepidium extensive field testing is necessary both draba L., Brassicaceae). A description of alone and in combination with the two this weed problem in the U.S. was previously described pathogens. Further presented in section 2.2.3. Although it is molecular characterization of the species not a problematic weed in Turkey, it has is also necessary. become a problematic weed in wheat growing regions of Tunisia (38). 3. COLLABORATION WITH TUNISIA Cercospora bizzozeriana Saccardo 3.1. Background. & Berlese. In 2002, dying L. draba plants Informal collaboration on with numerous leaf spots were found in a biological control of weeds with plant field in Tunis, Tunisia. The fungus pathogens between FDWSRU and Cercospora bizzozeriana was isolated Tunisia began in 2001 through scientist- from diseased leaves (64) and diseased to-scientist contacts with Dr. T. Souissi of tissue and cultures were sent to the the Institut National Agronomique de quarantine facility at FDWSRU for host- Tunisie (INAT) and Dr. K. Latiri of the range determination testing. Meanwhile, Institut National de la Recherche plots of L. draba were spray inoculated Agronomique de Tunisie (INRAT). with spores of C. bizzozeriana at Sidi Formal collaboration began in 2002 with Bouzid, Tunisia. The number of diseased a three-year project between FDWSRU, plants out of the total number of plants in INAT and INRAT funded by the USDA the plot (disease incidence) and the Foreign Agricultural Service (FAS). A number of diseased leaves out of the total three-year extension to the original number of leaves on diseased plants project was funded by FAS for 2005 (disease severity) were recorded every through 2007. After the project two weeks. The average disease incidence terminated, informal collaboration has at 42 days after inoculation was 26 + 3% continued, until now, between FDWSRU and the average severity on diseased and both institutes. plants was 45 + 7% at that time. Although these results were encouraging, results of 3.2. Weed targets and pathogens host-range testing at FDWSRU indicated for biological control of weeds in the that a few cultivated species of U.S. and Tunisia. Brassicaceae were susceptible to the A total of 65 disease specimens fungus and that the host-range was too were collected from 12 different genera Tunisian Journal of Plant Protection 58 Vol. 6, No. 1, 2011 broad to warrant further testing in either crops (50). It spreads rapidly, is highly country. competitive, and is difficult to control, This fungus seems to be widely particularly in rangelands and pastures. In distributed in the native range of the weed these ecosystems, a biological control and probably exerts some natural control agent is needed. pressure on the weed. It has been found not only in Tunisia but also in Russia (54) Puccinia carduorum Jacky. Isolates and Greece (data not published). Disease of this rust fungus have been evaluated specimens from Tunisia and Russia were extensively as potential biological control deposited in the U.S. National Fungus agents of Carduus thistles (19, 59). One Collection as BPI 843753 and BPI isolate of this fungus was successfully 878175, respectively, and ITS sequences introduced to the U.S. to control C. for the two isolates were deposited in nutans (13) while another isolate was GenBank as accession #s DQ370428 and found parasitizing C. tenuiflorus in EU031780, respectively. California (75). However, neither isolate Although not previously causes significant disease on IT in the reported in the U.S., C. bizzozeriana had U.S. (19, 75). Thus, there is a need to been previously reported on L. draba in discover an isolate of this fungus that is Manitoba, Canada (14). It was hoped that virulent and aggressive on IT in the U.S. the more recent report of the fungus During plant disease surveys, causing disease on L. draba (64) might from 2003 to 2005, in Northern Tunisia, encourage researchers to re-investigate numerous geographical isolates of rust the possible occurrence of the fungus in identified as Puccinia carduorum (Fig. 6) the U.S. Diseased leaves of L. draba were were collected (51). collected near Shepherd, Montana in Although IT collections from the 1997 and 2007, and the causal agent was U.S. were not found susceptible to these identified as C. bizzozeriana (22). Now isolates, one isolate (BPI No. 878207, that the fungus has been reported in the GenBank accession # EF050059) was U.S., there might be an opportunity to use used in subsequent disease progress and it in an inundative biological control yield loss studies in Tunisia (50). It was program if the non-target effects can be found that IT plants in the 2-5 leaf growth adequately addressed. stage were most susceptible to the rust and that multiple urediniospore 3.2.2. Italian thistle (IT) ( Carduus inoculations, mimicking secondary pycnocephalus L., Asteraceae). Italian disease cycles, reduced root and rosette thistle is a winter annual weed that is dry weights by 66 and 70%, respectively, native to North Africa and Eurasia (70) compared to controls (50). Thus, but is now widespread in the temperate appropriately timed applications of regions of the world (60). It is an urediniospores could provide biological introduced invasive weed in 10 states in control of this weed in Tunisia. To enable the U.S. and has been declared noxious in a biological control project for this weed 5 states (71). It is a target of biological in Tunisia, external funding is necessary control efforts in the U.S. (60). In to purchase spore harvesting and Tunisia, this weed is probably native, but application equipment and establish rust it has become widely-distributed in the spore multiplication plots. This, in turn, North of Tunisia and can be found in could lead to a successful small-scale rangelands and pastures as well as in biological control industry in Tunisia.
Tunisian Journal of Plant Protection 59 Vol. 6, No. 1, 2011
Fig. 6. Rust on Carduus pycnocephalus caused by Puccinia carduorum in a field in Tunisia.
4. COLLABORATION WITH 4.2. Weed targets and pathogens GREECE for biological control of weeds in the 4.1. Background. U.S. and Greece. Informal collaboration with A total of 155 disease specimens Greece began in 2001 with scientific were collected from 34 different genera visits by the senior author to the USDA, and 44 species of weeds from 2001 to ARS, European Biological Control 2010 in Greece. From these diseases, 38 Laboratory (EBCL) substation in pathogens were isolated and identified at Thessaloniki, Greece. Formal least to genus. Of these pathogens, six, collaboration with Greece began in 2003 that were not isolated elsewhere, were with a three-year specific cooperative judged to be promising potential agreement between USDA, ARS, biological control agents for weeds in the FDWSRU and American Farm School U.S. (classical biological control) and/or (AFS), Thessaloniki, Greece. A two-year Greece (inundative biological control). extension to the original project was Descriptions of the target weeds and the funded by USDA, ARS for 2006-2008. status of development of these promising AFS is also the campus of the EBCL potential control agents follow. substation in Greece. In 2010, EBCL funded a collaborative effort on 4.2.1. Yellow starthistle (YST) biological control of weeds with plant (Centaurea solstitialis L., Asteraceae). pathogens between FDWSRU and Yellow starthistle is a winter annual weed Aristotle University in Thessaloniki, that can form dense impenetrable stands Greece. in the U.S. It was introduced to the U.S.
Tunisian Journal of Plant Protection 60 Vol. 6, No. 1, 2011 in the 1800s and has been estimated to the fungus led to a description of a new infest up to 8 million hectares in species, C. centaureicola (11). A California alone (27). YST is native to specimen of the fungus has been North Africa and Eurasia (70) but is now deposited in the U.S. National Fungus present in 43 states in the U.S. It has been Collections Beltsville, Maryland declared a noxious weed in 12 Western (BPI844247) and the Centraalbureau voor states (71) and has long been a target of Schimmelcultures collection (CBS biological control efforts in the U.S. (27). 120253). The ITS sequence has been It is not an agricultural problem in deposited in GenBank, accession number Greece. AY961596 (see also EU019257.3). This fungus, like Septoria lepidii (section 4.2.1.1. Cladosporium herbarum 2.2.3.1) and Cercospora bizzozeriana (Pers.:Fr.) Link. (teleomorph = Davidiella (section 3.2.1.1) is likely widely tassiana (De Not.) Crous & U. Braun). In distributed in the native range of the 2003, an epidemic of dying YST plants plant, as another isolate was found on was found along the Galami-Kozani road YST in the Krasnodar region of Russia near Kozani, Greece. The pathogen (data not published), and likely exerts isolated from diseased plants was some natural control pressure. Host-range identified as Cladosporium herbarum (8, testing is on-going at FDWSRU, and field BPI 863446). When inoculated onto YST tests are planned for Greece. plants in a greenhouse, this pathogen proved to be extremely aggressive on 4.2.2. Russian thistle (RT) ( Salsola YST plants and readily moved from tragus L., Chenopodiaceae). Russian inoculated plants to non-inoculated thistle, or tumbleweed, is one of 11 plants, causing disease on both. Diseased species of Salsola in the U.S. All of these plants were very stunted with many species and their hybrids are introduced desiccated leaves by 21 days after from Eurasia (70). S. tragus is one of the inoculation. Most plants, both inoculated most invasive of these species in the U.S. and non-inoculated, that became diseased and is present in 48 states, although it is died. However, tests in quarantine at only declared noxious in three states (71). FDWSRU showed that the fungus had a RT is also a problem in some host range that was too broad to warrant agroecosystems in Greece (29). Chemical further testing in consideration for release herbicides are useful for management of in the U.S. RT in row crop agriculture, but this strategy is not practical for most of the 4.2.1.2. Cercosporella centaureicola infestation for ecological, economical, D. Berner, U. Braun & F. Eskandari, sp. and practical reasons, the latter because nov. In the spring of 2004 another infestations are often very large and occur epidemic of dying YST plants was found in pastures and grazing lands. For these near Kozani, Greece. Most of the lower reasons, classical biological control of leaves of rosettes of YST had many this weed by plant pathogens is under small, brown leaf spots. In many cases, investigation as a potential management these spots coalesced and resulted in tool (5). necrosis of many of the leaves and death of the rosette. The fungus isolated from Colletotrichum gloeosporioides f. the leaf spots was identified as a sp. salsolae (Penz.) Penz. & Sacc. in Cercosporella sp. (32). Further tests with Penz. (teleomorph = Glomerella
Tunisian Journal of Plant Protection 61 Vol. 6, No. 1, 2011 cingulata [Stoneman] Spauld. & H. specific and not damaging to non-target Schrenk) (CGS). A number of isolates of species (25, 41, 53, 67). One such isolate Colletotrichum gloeosporioides have from Hungary (62) has been shown to be been evaluated for biological control of lethal to S. tragus , with a very specific weeds, despite the fact that C. host range (6, 17). Isolates genetically gloeosporioides has been reported from similar (identical ITS sequences) to the many hosts (33). However, some isolates Hungarian isolate were also found in of C. gloeosporioides, which have been Greece (9, Fig. 7) and Russia (43). used for biological control, are host-
Fig. 7. Epidemic of dying Salsola tragus plants along a beach on the Aegean Sea in Greece. The pathogen isolated from the disease was Colletotrichum gloeosporioides f. sp. salsolae.
As with several other pathogens specimens and ITS sequences of the previously discussed, the fungus appears isolates were deposited in the U.S. to be widespread in the native range of S. National Fungus Collections and tragus and probably exerts some natural GenBank as BPI 871126, GenBank control pressure on the weed. Discovery accession # DQ344621 (Greece) and BPI of the isolates in Greece and Russia has 878389, GenBank accession # EU530697 made field tests, with the results directly (Russia). A petition to the Animal and applicable to the Hungarian isolate, Plant Health Inspection Service (APHIS) possible. Initial results from of USDA to release the fungus in the U.S. epidemiology tests in the field suggest is being drafted. that, given adequate rainfall, disease severity, resulting from artificial 4.2.3. Milk thistle (MT) ( Silybum inoculation, reaches 100% within two marianum (L.) Gaertn., Asteraceae). months of inoculation and that carry-over Milk thistle is an erect winter inoculum into subsequent growing annual (or biennial) weed that grows from seasons eliminates stands of RT. Disease 1-2 m tall and forms dense, impenetrable
Tunisian Journal of Plant Protection 62 Vol. 6, No. 1, 2011 stands (4). It is a native of North Africa powdery masses of teliospores were and Eurasia (70) and is present in 27 U.S. found in all ovaries and florets. All of the states and is declared noxious in three capitula on diseased plants were similarly states (71). It is a target of biological diseased, and no seeds were found from control efforts in the U.S. and was one of diseased plants (Fig. 8). As all capitula the targets for the release of the seed and florets on diseased plants were weevil Rhinocyllus conicus in California diseased, the disease appears to be (35). It is not generally considered an systemic. The smut fungus was newly agricultural problem in Greece. described as Microbotryum silybum (72). A specimen has been deposited in the Microbotryum silybum Vánky & U.S. National Fungus Collection, BPI Berner, sp. nov. In 2001, during a 863477, and ITS sequences in GenBank, collection trip to find potential pathogens (accession # AY285774). Inoculation of of MT, numerous smutted flower heads the fungus on MT in the field in Greece (capitula) of MT were found in a weedy resulted in 90% diseased plants with all field in south-eastern Greece. When ovaries replaced by teliospores (Fig. 8). smutted capitula were split open,
Fig. 8. (A) Capitulum of Silybum marianum diseased with Microbotryum silybum. All florets are filled with smut teliospores resulting in no seed production, (B) Field plot in Greece of Silybum marianum plants artificially inoculated with M. silybum . All capitula of 90% of the plants are systemically diseased with M. silybum ; note the swollen capitula with no flower production.
In 2005, about 25% of MT plants in plants had decreased by 83% from the a MT infested field at AFS were peak density and 40% of the remaining artificially inoculated with M. silybum. MT plants were systemically diseased. The proportion of diseased plants and the This level of weed control indicates that total number of MT plants was thereafter M. silybum is potentially a good recorded each year for five years; there biological control agent for MT. Host were no subsequent inoculations. At the range determination is underway in end of this time, the total number of MT quarantine at FDWSRU, but this is a
Tunisian Journal of Plant Protection 63 Vol. 6, No. 1, 2011 difficult task since many native, related, 4.2.4. Italian thistle (IT) ( Carduus Cirsium spp. in the U.S. rarely flower in pycnocephalus L., Asteraceae). This quarantine greenhouses. Since the fungus weed was described in section 3.2.2. IT is is an ovary smut, no disease can be not an agricultural problem in Greece. observed on plants that do not flower. Microbotryum silybum Vánky & Some of the species could be tested in the Berner, sp. nov. In 2005, smutted IT field in Greece, but many of these species plants (Fig. 9) were also found in the are not native to Greece. This presents a same field as smutted MT plants. quarantine problem in Greece that has not been solved.
Fig. 9. (A) Capitula of Carduus pycnocephalus smutted with Microbotryum silybum in the field in Greece. Note the swollen shape of the capitula and the teliospores in the split capitulum, (B) Capitula of C. pycnocephalus smutted with M. silybum in a quarantine greenhouse at FDWSRU.
The fungus was initially described silybum on IT presents an interesting as a Microbotryum sp. (10), but alignment possibility of controlling two target of the ITS sequences (GenBank accession weeds with the same biological control #AY280460) with the sequences from M. agent. Host range testing of this fungus silybum showed that there were two gaps was discussed in the previous section. A resulting in 616 out of 618 identities or specimen of the fungus from IT has been 99.67% similarity. Inoculations in deposited in the U.S. National Fungus quarantine at FDWSRU of MT plants Collection as BPI 871812. with teliospores from the IT isolate resulted in disease as did inoculations of 4.2.5. Common crupina (CC) IT plants with teliospores from MT. (Crupina vulgaris Cass., Asteraceae). These two isolates seem likely to be the Common crupina is native to North same fungus. The discovery of M. Africa and Eurasia (70) but it is
Tunisian Journal of Plant Protection 64 Vol. 6, No. 1, 2011 introduced and has become invasive in Puccinia crupinae (30). Tests are California, Oregon, and Washington currently being conducted at FDWSRU states, the only states where it has been for host range and efficacy of this fungus. reported in the U.S. It has been declared a This is only the third report of this rust on federal noxious weed (70) and movement CC in the world (33). Initial results from of plant materials is restricted and tests at FDWSRU show that the fungus is regulated by permit. It is a target of aggressive on CC (Fig. 10) and that the biological control efforts in the U.S. but host range might be narrow enough for is not problematic in Greece. the rust to be used as a biological control agent in the U.S. A specimen has been Puccinia crupinae Ranojevic. In deposited in the U.S. National Fungus 2001, a rust fungus was found on CC near Collection as BPI 880889 and ITS Kozani, Greece. Specimens were sent to sequences have been deposited in the quarantine laboratory at FDWSRU, GenBank, accession # HQ184334. and the fungus was later identified as
Fig. 10. Rust caused by Puccinia crupinae on Crupina vulgaris in a quarantine greenhouse at FDWSRU.
4.2.6. Canada thistle (CT) Europe. CT has now spread to 38 states in (Cirsium arvense (L.) Scop.), the U.S. and has been declared noxious in Asteraceae). CT, also known as 25 (39), making it one of the most widely California thistle and creeping thistle, is a declared noxious weeds in the U.S. It is serious problematic weed of pastures, also an agricultural problem in Greece rangelands and agricultural lands (28). throughout the temperate areas of the world (2, 52). CT is a creeping perennial Puccinia punctiformis (F. Strauss) that is native to southeastern Europe and Rohl. P. punctiformis was perhaps the North Africa and is believed to have been first plant pathogen proposed as a introduced to North America from biological control agent for CT or any
Tunisian Journal of Plant Protection 65 Vol. 6, No. 1, 2011 other weed; it is commonly found Jersey farmer noticed Canada thistle everywhere that CT is found. The fungus patches diseased with the rust virtually is an obligate, autoecious, branchy-form disappeared after a couple of years, and rust that can systemically infect Canada he proposed that the rust be widely thistle (34, Fig. 11). In 1893, a New disseminated to control the weed (77).
Fig. 11. Cirsium arvense plant systemically diseased by Puccinia punctiformis . Spores on the leaves are predominantly urediniospores with intermixed teliospores.
In 1915, Cockayne (24) in New through this collaboration, successful Zealand also proposed that the rust be biological control of CT can be used for biological control of the thistle, established in both countries. but stated that it was exceedingly difficult to collect enough teliospores for 5. COLLABORATION WITH inoculation. FDWSRU is in the process RUSSIA of overcoming the teliospore limitations 5.1. Background. and is attempting to routinely establish Formal collaboration with systemic P. punctiformis infections and Russia began in 2005 with a three-year rust by inoculations of plants in the field International Science and Technology with teliospores. Field inoculations, Center (ISTC) project between following protocols established at FDWSRU, The All Russia Rice Research FDWSRU, are now also being Institute (ARRRI) in Krasnodar, Russia, implemented in Greece with Greek The All Russia Phytopathology Research isolates of the rust. It is hoped that Institute (ARPRI) in Moscow, Russia, Tunisian Journal of Plant Protection 66 Vol. 6, No. 1, 2011 and the Department of Genetics and collaboration described in this manuscript Breeding, St. Petersburg State University, is based. St. Petersburg, Russia. A three-year 5.2.1.1. Phomopsis oblonga (Desm.) extension to the original project was Traverso (teleomorph = Diaporthe eres funded by ISTC for 2008-2011. Nitschke). In 2007, dying RT plants were found along the Azov Sea in Russia. The 5.2. Weed targets and pathogens fungus isolated from the diseased plants for biological control of weeds in the was Phomopsis oblonga (teleomorph = U.S. and Russia. Diaporthe eres ) (42). In field and A total of 77 disease specimens greenhouse tests, the fungus has been were collected from 15 different genera shown to be very aggressive on RT and a and 22 species of weeds from 2005 to potential biological control agent for this 2010 in Russia. From these diseases, 19 weed. Host range testing is in progress at pathogens were isolated and identified at FDWSRU and some field tests have been least to genus. Of these pathogens, four, completed in Russia. A specimen has that were not isolated elsewhere, were been deposited in the U.S. National judged to be promising potential Fungus Collection as BPI 878717 and biological control agents for weeds in the ITS sequences have been deposited in U.S. (classical biological control) and/or GenBank, (accession # EU805539). Russia (inundative biological control). Descriptions of the target weeds and the 5.2.1.2 Uromyces salsolae status of development of these promising Reichardt. In 2005, rusted RT plants were potential control agents follow. found on a beach along an inlet to the Azov Sea in Russia. The rust fungus 5.2.1. Russian thistle (RT) ( Salsola isolated from the diseased plants was tragus L., Chenopodiaceae). This weed identified as Uromyces salsolae. This rust was described in section 4.2.2. It is not causes extensive damage to RT (Fig. 12) considered an agricultural problem in the and is a good candidate biological control areas of Russia where the mutual agent.
Fig. 12. Salsola tragus diseased by the rust fungus Uromyces salsolae in a quarantine greenhouse at FDWSRU.
Tunisian Journal of Plant Protection 67 Vol. 6, No. 1, 2011
Host range testing of the rust began U.S. National Fungus Collection as BPI in 2005, and the fungus has been found to 878355 and ITS sequences have been be specific to Salsola spp. (5) with no deposited in GenBank, (accession # susceptible related taxa. There are no EU367468). native Salsola in North America. A petition to release the fungus in the U.S. 5.2.3. Barnyard grass (BG) has been submitted to APHIS and is (Echinochloa crus-galli (L.) Beauv., pending approval. A specimen has been Poaceae). BG is one of the world’s worst deposited in the U.S. National Fungus weeds, particularly so in rice producing Collection as BPI 878751 and ITS areas (37). BG is very competitive with sequences have been deposited in rice and can significantly reduce rice GenBank, (accession # EU872159). yields (63). This weed is the primary pest in the Krasnodar rice producing area of 5.2.2. Yellow starthistle (YST) Russia (45). However, due to increasing (Centaurea solstitialis L., Asteraceae). costs of rice production in this area, This weed was described in section 4.2.1. alternatives to chemical herbicides are It is not an agricultural problem in Russia. actively being sought.
Periconia igniaria E.W. Mason & Ustilago trichophora (Link) Kunze. M.B. Ellis (teleomorph = In 2006, smutted spikelets of BG Didymosphaeria igniaria C. Booth). In were found at the ARRRI (Fig. 13a). The the summer of 2006, several hundred fungus isolated from the spikelets was severely diseased YST plants were found identified as Ustilago trichophora . near Taman, Russia. Symptoms of the Teliospores of the fungus, from diseased disease were yellow water-soaked leaf spikelets, were sent to the ARPRI where spots. Diseased leaves were collected and the teliospores were germinated and the sent to the Russian State Collection of sporidia of the fungus cultured. Sporidia Phytopathogenic Organisms at ARPRI. were then mass-produced in liquid culture The fungus isolated from the diseased and used to inoculate tillers of BG. leaves was identified as Periconia Diseased tillers, from these inoculations, igniaria (44). Field tests on YST with produced numerous fungus galls spray inoculation of P. igniaria were containing masses of teliospores (Fig. conducted in 2007. The fungus is an 13b). Diseased tillers eventually died. It is extremely aggressive pathogen on YST, this state of the disease i.e. tiller disease and all field-inoculated plants were killed that is potentially important for biological within 10 days after inoculation. Results control of BG, as diseased tillers of field inoculations resembled eventually die and masses of teliospores application of a chemical herbicide. Host are released from smut galls to infect range testing is in progress at FDWSRU. nearby plants. A specimen has been deposited in the
Tunisian Journal of Plant Protection 68 Vol. 6, No. 1, 2011
Fig. 13. (A) Swollen spikelets of Echinochola crus-galli diseased by Ustilago trichophora , (B) Tillers of E. crus-galli diseased by U. trichophora ; the smut galls are filled with teliospores of the fungus.
Field tests are underway with this collaborators. These projects in Turkey, fungus in Russia to find effective ways to Tunisia, Greece, and Russia have resulted use mass-produced sporidia to infect BG in discoveries of many new diseases of on a large scale. Numerous isolates of this weeds which, in turn, have led to fungus have been reported from around numerous reports of newly discovered the world, including the U.S., and there pathogens from these weeds. In each are many specimens in the U.S. National country, these newly discovered Fungus Collection (33). The ITS pathogens are being, or have been, tested sequences for this isolate were deposited in the field and laboratory for in GenBank (accession # HQ201379). effectiveness in relation to environmental variables and host-range for potential 6. CONCLUSION release and use in the respective countries Formalized international and the U.S. In each country, at least one collaboration, through funded projects, on pathogen, discovered from these biological control of weeds with plant collaborative activities, is being evaluated pathogens is an effective, legal, and for use as an inundative biological control ethical way of discovering and collecting agent in that country. In all of these new weed pathogens that can be used as countries, biological control of weeds classical biological control agents in the with plant pathogens is a relatively new U.S. and inundative biological control scientific endeavor, but as individual agents in the countries of origin of the reports of new pathogens and their weed and pathogen. Collaborative potential appear in the literature, projects from 2001-2010 on biological administrators are becoming more aware control of weeds with plant pathogens of the overall potential of this approach. have resulted in long-term collaboration As administrators and other scientists and mutual benefits for all of the become convinced of the value of Tunisian Journal of Plant Protection 69 Vol. 6, No. 1, 2011 biological weed control in their respective these biological control agents. In turn, countries, more funding might be directed successful projects, at the local level, will at individual biological control projects. lead to increasing interest and funding in Given more local funding, and hopefully biological weed control in general and to more international funding, many of these sustained collaboration with biological inundative biological control projects can weed control programs in the U.S. come to fruition i.e. release and use of ______
RESUME Berner D., Souissi T., Smallwood E., Cavin C., Eskandari F., Tunali B., Buyuk O., Yildirim A., Mukhina Z., Kolomiets T., Matveeva T., Bogomaz D., Kassanelli D., Mejri D., Latiri K., Kashefi J. et Lagopodi A. 2011. Avantages mutuels issus des collaborations internationales pour la lutte biologique contre les mauvaises herbes moyennant des phytopathogènes. Tunisian Journal of Plant Protection 6: 49-74.
Aux Etats Unis, les mauvaises herbes envahissantes ont des effets catastrophiques sur les écosystèmes agricole, aquatique, riverain, naturel et les parcours. Pour ces trois derniers, la lutte biologique classique au moyen des ennemies naturels introduits à partir des pays d’origine, y compris les phytopathogènes, est en général le seul moyen de lutte qui soit économique contre ces mauvaises herbes. Afin de poursuivre la lutte biologique classique au moyen des phytopathogènes, l’unité de recherche des maladies exotiques-malherbologie (FDWSRU) de l’USDA-ARS s’appuie sur des collaborations internationales avec des chercheurs dans les pays d’origines des mauvaises herbes cibles. Les résultats de ces collaborations sont rapportés dans cet article pour mettre en évidence les avantages mutuels issus de collaborations internationales pour la lutte biologique contre les mauvaises herbes au moyen de phytopathogènes. Pendant plus de 30 ans, FDWSRU a conduit avec succès des travaux de recherche sur la lutte biologique classique contre les mauvaises herbes envahissantes au moyen des phytopahtogènes. Cependant, pour découvrir de nouvelles accessions de pathogènes de mauvaises herbes, il est essentiel d’établir des collaborations avec des chercheurs dans les pays d’origine des mauvaises herbes cibles qui souvent, ne sont pas impliqués dans de telles activités de recherche pour plusieurs raisons dont l’absence de financement. Actuellement et en raison d’une demande de plus en plus croissante de la part des agriculteurs (et des consommateurs) pour une gestion de mauvaises herbes efficace, non coûteuse et respectueuse vis-à-vis de l’environnement, d’une augmentation de la production biologique, du développement de la résistance herbicide chez plusieurs espèces de mauvaises herbes et d’une prise de conscience de l’impact des herbicides sur l’environnement et la santé humaine, les mycoherbicides et la lutte biologique inondative sont devenus des alternatives aux herbicides et gagnent de plus en plus d’intérêt à travers le monde. En conséquence, plusieurs projets de collaboration ont été élaborés durant les 10 dernières années entre FDWSRU et des chercheurs internationaux. Ces projets internationaux avec la Turquie, la Tunisie, la Grèce et la Russie ont abouti à la découverte de nombreuses maladies de mauvaises herbes qui, à leur tour ont conduit à de nombreux rapports sur les agents pathogènes nouvellement décrits sur ces mauvaises herbes. Les données scientifiques sur de nouveaux pathogènes et leurs potentiels peuvent attirer l’attention des décideurs qui seront de plus en plus disposés à soutenir de nouveaux projets de lutte biologique contre les mauvaises herbes.
Mots clés: Collaboration internationale, lutte biologique classique, lutte biologique inondative, mauvaises herbes, mycoherbicides, pathogènes. ______
Tunisian Journal of Plant Protection 70 Vol. 6, No. 1, 2011
______
ر ، دا و و أ ود وآ اغ آ و ر ر ري و ر وأوره ن وأ ل ر وز ّ و را آ و ود ز ودا آ ودر ف ي وآ ي و آ وأ ز دي . 2011 . ا ا د ا ا ون ا و ان ا ا / ا ب ا رة ا ا ا ا . Tunisian Journal of Plant Protection 6: 49-74.
ا ب ا ز ا ُ إ ا ت ا ة ر آ ر ُ ُ ا ا وا وا وا . و ُ ُ ا ا ة، و أن إد ل ا اء ا ، ذ ا ت آ ا اع ا أ و ً، ا ا ا ا ا ا د ً ء ه ا ب . و ا ار ا ا ا ا ب ا رة ا ا ا ت، و ة ث أ اض ا ب ا رة ا ( FDWSRU ) ا ـ USDA-ARS ا ون ا و ان ا ا ب از ا ا د ا آ ه ا ا ون ا ب ا رة ا ا ا ُ ْ . ا ة FDWSRU ح ل أآ ا ا ا ب ا رة ا ا ا . أ إ ون ان ا ب ا رة ا آ ف ُ ت ة ا ا ا ب ا رة ، وا ا ، ، ا دة ا ا ع ا ث ب دة ب ا . و ا ة ا و اً ا ا ة ف ا ( وا ) أ ا وأ ا ب، و ز دة ا ج ا را ا و ز دة ا د ا ام ات ا ب و ز دة ّ ر ا و ى ا أ اع ا ب ا رة ات ا ب، أ ا ا ا ا وا ات ا ب ا رة ا ا ات ا ب ا وأ ه م ا ى ا ا ء ا . و ه ا ا ه م ا دل ا إ ار ة ر و ر ، ل ا ات ا ة ، FDWSRU و دو . . و أدت ه ا ر ا و آ و وا ن ورو ا اآ ف ا أ اض ا ب، وا دت وره إ ا ر ا ا ا ُ ْ ا ً ه ا ب ا رة، و ر ه ا ر ا ور ت ا ، أ ا دار ن درا ا ا ا وأآ ر ر ة ا إزاء ا ب ا رة.
آ ت : ا ب ا رة، ا ون ا و ، ُ ْ ت ا ب ، ا ا / ا ا ا ، ا ا / ا ا ، ات ب
______
LITERATURE CITED 1. Agrios, G.N. 2005. Plant Pathology, Fifth 5. Berner, D.K., Bruckart, W.L., Cavin, C.A., and Edition. Elsevier Academic Press, Burlington, Michael, J.L. 2009a. Mixed model analysis MA, 922 pp. combining disease ratings and DNA sequences 2. Amor, R.L. and Harris. R.V. 1974. Distribution to determine host range of Uromyces salsolae and seed production of Cirsium arvense (L.) for biological control of Russian thistle. Scop. in Victoria, Australia. Weed Res. 14: Biological Control 49: 68-76. 317-323. 6. Berner, D.K., Bruckart, W.L., Cavin, C.A., 3. Andrianova, T.V. and Minter, D.W. 2001. Michael, J.L., Carter, M.L., and Luster. D.G. Septoria lepidii . International Mycological 2009b. Best linear unbiased prediction of host Institute Descriptions of Fungi and Bacteria range of the facultative parasite Colletotrichum 1417: 1-2. gloeosporioides f. sp. salsolae , a potential 4. Bean, C. 1985. Silybum marianum , blessed milk biological control agent of Russian thistle. thistle. Element Stewardship Abstract. In: The Biological Control 51: 158-168. Nature Conservancy. Available from: 7. Berner, D.K., Dubin, H.J., and Smallwood, E.L.
smut caused by Ustilago phrygica from Turkey. from Carduus thoermieri, C. tenuiflorus , and C. Plant Dis. 91: 906. pycnocephalus . Phytopathology 81: 192-197. 8. Berner, D.K., Smallwood, E.L., McMahon, 20. Bruhn, C.M., Diaz-Knauf, K., Feldman, N., M.B., Luster, D.G., and Kashefi, J. 2007b. First Harwood, J., Ho, G., Ivans, E., Kubin, L., report of leaf spot caused by Cladosporium Lamp, C., Marshall, M., Osaki, S., Stanford, G., herbarum on Centaurea solstitialis in Greece. Steinbring, Y., Valdez, I., Williamson, E., and Plant Dis. 91: 463. Wunderlich, E. 1992. Consumer food safety 9. Berner, D.K., Cavin, C.A., McMahon, M.B., concerns and interest in pesticide-related and Loumbourdis, I. 2006a . First report of information. J. Food Safety 12: 253-262. anthracnose of Salsola tragus caused by 21. Carpenter, A.T. and Murray, T.A. 1998. Colletotrichum gloeosporioides in Greece. Acroptilon repens (L.) De Candolle ( Centaurea Plant Dis. 90: 971. repens (L.) Russian knapweed. Element 10. Berner, D.K., McMahon, M.B., Kashefi, J., and Stewardship Abstract. In: The Nature Erbe, E. 2006b. First report of an ovary smut of Conservancy. Available from: Italian thistle caused by a Microbotryum sp. in
32. Eskandari, F.M., Berner, D.K., Kashefi, J., and by Colletotrichum gloeosporioides in Russia. Strieth, L. 2004. First report of leaf spot caused Plant Dis. 92:1366. by Cercosporella sp. on Centaurea solstitialis 44. Kolomiets, T., Pankratova, L., Mukhina, Z., in Greece. Plant Dis. 88: 1382. Kassanelly, D., Matveeva, T., Bogomaz, D., 33. Farr, D.F. and Rossman, A.Y. 2010. Fungal and Berner, D. 2008b. First report of leaf spot Databases, Systematic Mycology and caused by Periconia igniaria on yellow Microbiology Laboratory, ARS, USDA. starthistle in Russia. Plant Dis. 92: 983. Available from: < http://nt.ars- 45. Kolomiets, T.M., Skatenok, O.O., Mukhina, grin.gov/fungaldatabases/> (accessed 14.08.10). Zh.M., and Berner, D.K. 2008c. Search of fungi 34. French, R.C. and Lightfield, A.R. 1990. – potential agents for biological control of weed Induction of systemic aecial infection in Canada plant Echinichloa crus-galli (L.) Beauv. Pages: thistle (Cirsium arvense ) by teliospores of 453-460. In 50 years on guidance of agricultural Puccinia punctiformis . Phytopathology 80: 872- safety of the country. Anniversary issue. 877. Bolshiye Vyasemy, Russia, 656 pp. 35. Goeden, R.D. and Ricker, D.W. 1977. 46. Kuleci, E., Tunali, B., Berner, D.K., Cavin, Establishment of Rhinocyllus conicus on milk C.A., and Castlebury, L.A. 2009. First report of thistle in southern California. Weed Sci. 25: leaf anthracnose caused by Phomopsis 288-292. convolvuli on field bindweed in Turkey. Plant 36. Heap, I. 2010. The International Survey of Dis. 93: 847. Herbicide Resistant Weeds. Available from: 47. Lyons, K.E. 1998a. Cardaria draba (L.) Desv., http://www.weedscience.org/In.asp (accessed heart-podded hoary cress , Cardaria chalepensis 16.08.10) . (L.) Hand-Maz., lens-podded hoary cress , and 37. Holm, L.G., Plucknett, D.L., Pancho, J.V., and Cardaria pubescens (C. A. Myer) Jamolenko, Herberger, J.P. 1977. The World's Worst globe-podded hoary cress. Element Stewardship Weeds. The University Press of Hawaii, Abstract. In: The Nature Conservancy. Honolulu. HI, 609 pp. Available from: 38. Jendoubi, H. 2004. Le cresson blanc ( Lepidium
55. Nielsen, J. 1992. Ustilago spp. pathogenic on hirta in Hawaiian forests. Plant Dis. 70: 974- Aegilops . III. Ustilago phrygica , with a 976. descriptive key to all three Ustilago spp. on 68. Tunali, B., Berner, D.K., and Dubin, H.J. 2008. Aegilops . Can. J. Bot. 70: 581-588. First report of leaf spot caused by 56. Ormeno-Nunez, J., Reeleder, R.D., and Watson, Colletotrichum cf. linicola on field bindweed in A.K. 1988a. A foliar disease of field bindweed Turkey. Plant Dis. 92: 316. (Convolvulus arvensis) caused by Phomopsis 69. Tunali, B., Eskandari, F.M., Berner, D.K., Farr, convolvulus . Plant Dis. 72: 338-342. D.F., and Castlebury, L.A. 2003. First report of 57. Ormeno-Nunez, J., Reeleder, R.D., and Watson, leaf blight caused by Phoma exigua on A.K. 1988b. A new species of Phomopsis Acroptilon repens in Turkey. Plant Dis. 87: recovered from field bindweed ( Convolvulus 1540. arvensis ). Can. J. Bot. 66: 2278-2233. 70. USDA, ARS, National Genetic Resources 58. Pfirter, H.A. and Defago, G. 1998. The Program. Germplasm Resources Information potential of Stagonospora sp. as a Network - (GRIN) [Online Database]. National mycoherbicide for field bindweed. Biocontrol Germplasm Resources Laboratory, Beltsville, Sci. Technol. 8: 93-101. Maryland. Available from:
Tunisian Journal of Plant Protection 74 Vol. 6, No. 1, 2011