Successful establishment of epiphytotics of Puccinia punctiformis for biological control of Cirsium arvense

Authors: Berner, Dana; Smallwood, Emily; Cavin, Craig; LAGOPODI, ANASTASIA - Aristotle University Of Thessaloniki; KASHEFI, JAVID - European Biological Control Laboratory (EBCL); KOLOMIETS, TAMARA - Russian Institute Of Phytopathology; PANKRATOVA, LYUBOV - Russian Institute Of Phytopathology; MUKHINA, ZHANNA - Russian Institute Of Phytopathology; CRIPPS, MICHAEL - Agresearch; BOURDOT, GRAEME - Agresearch

Submitted to: Biological Control
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 9/11/2013
Publication Date: 12/1/2013
Publication URL: http://handle.nal.usda.gov/10113/57956
Citation: Berner, D.K., Smallwood, E.L., Cavin, C.A., Lagopodi, A., Kashefi, J., Kolomiets, T., Pankratova, L., Mukhina, Z., Cripps, M., Bourdot, G. 2013. Successful establishment of epiphytotics of Puccinia punctiformis for biological control of Cirsium arvense. Biological Control. 67:350-360.

Interpretive Summary: Canada thistle (CT) is one of the worst weeds in temperate areas of the world. A rust fungus was first proposed as a biological control agent for CT in 1893. The rust causes systemic disease, is specific to CT, and is in all countries where CT is found. Despite a 120-year lapse since biological control with the rust was proposed, attempts at routine establishment of systemic rust disease in the field have previously been unsuccessful due to incomplete understanding of the disease cycle. In this study, newly-emerging CT seedlings in the fall are proposed as the infection site that gives rise to systemically diseased shoots the following spring. To test this hypothesis, seedlings of CT were inoculated in the fall with leaves containing rust spores collected in mid-summer. Field sites were located near Kozani, Greece, Moscow, Russia, Christchurch, New Zealand, and Ft. Detrick, Maryland, USA. Temperature and dew conditions at inoculation in the fall at each site were very favorable for spore germination. Inoculations of CT seedlings in all 13 sites produced systemically diseased shoots. A separate study showed that the maximum rate of CT leaf drop occurred at the time of maximum emergence of new CT seedlings in the fall. This period coincided with an annually occurring period of sustained dew and favorable temperatures for spore germination. This study demonstrates that systemic rust disease of CT can be routinely established, by mimicking the natural disease cycle.

Technical Abstract: Canada thistle (Cirsium arvense, CT) is one of the worst weeds in temperate areas of the world. The rust fungus Puccinia punctiformis was first proposed as a biological control agent for CT in 1893. The rust causes systemic disease, is specific to CT, and is in all countries where CT is found. Despite a 120-year lapse since biological control with the rust was proposed, establishment of epiphytotics of the rust have previously been unsuccessful due to incomplete understanding of the disease cycle. In this study, newly-emerging rosettes in the fall are proposed as the physical and temporal infection courts for basidiospores, from germinating teliospores, to systemically infect CT and give rise to systemically diseased shoots the following spring. To test this hypothesis, rosettes of CT were inoculated in the fall with either telia-bearing leaves collected in mid-summer or with greenhouse-produced teliospores. Telia-bearing leaves, which were used as inoculum in 12 of 13 field sites, were collected from CT shoots near systemically diseased CT shoots producing aeciospores in the spring. Aeciospore infections of these leaves gave rise to uredinia which turned to telia in mid-to-late-summer. Field sites were located near Kozani, Greece, Moscow, Russia, Christchurch, New Zealand, and Ft. Detrick, Maryland, USA. Temperature and dew conditions at inoculation in the fall at each site were very favorable for teliospore germination. Rosettes inoculated in the fall were marked with flags, and systemically diseased shoots emerging near these flags the following spring were recorded. In 11 of the sites in these countries, individual rosettes were inoculated 2, 4, 6, or 8 times with telia-bearing leaves. Proportions of rosettes giving rise to systemically diseased shoots, out of the number of rosettes inoculated, were analyzed. Inoculations in all 13 sites produced systemically diseased shoots. A separate study on the phenology of CT showed that the maximum rate of leaf abscission occurred at the time of maximum emergence of new CT rosettes in the fall. This period coincided with an annually occurring period of sustained dew and favorable temperatures for teliospore germination. In nature, abscising telia-bearing leaves likely come into contact with a receptive rosette during favorable conditions for teliospore germination in the fall. This study demonstrates that epiphytotics of systemic rust disease of CT can be routinely established, by mimicking the natural disease cycle.