First Report of Black Swallow-Wort as an Alternate Host of the Two-Needle Pine Stem Rust Pathogen, Cronartium flaccidum, in France.

Abstract

Stem rust disease, caused by Cronartium flaccidum (Alb. & Schwein.) G. Winter, is among the most destructive diseases of the two-needle hard pine in the Northern Hemisphere, including Scots pine but also several Mediterranean pines in southern Europe (2,3). This heteroecious rust has numerous alternate herbaceous hosts spanning different plant families, thereby contributing to epidemic outbreaks when environmental conditions for infection are optimal (2,3). The main alternate host in Europe is the white swallow-wort, Vincetoxicum hirundinaria Medik, a herbaceous perennial in the milkweed family (Asclepiadaceae). At the southwestern edge of its distribution, V. hirundinaria co-occurs with the black swallow-wort, V. nigrum (L.) Moench and cases of misidentification between the two species are not uncommon. Little to no disease occurs to V. nigrum likely because phenanthroindolizidine alkaloid antimicrobial compounds are produced in the weed. In 1918, occurrence of C. flaccidum was reported in Spain and Portugal on black and white swallow-worts albeit as C. asclepadium (1). In the early summer of 2011, at Saint Clément de Rivière in southern France, we detected orange-yellow rust pustules on the lower leaf surfaces of several black swallow-worts growing near Aleppo pines (Pinus halepensis). These orange-yellow pustules were erumpent uredinia in groups (range = 137 to 400 μm in diameter) with peridia that broke with the production of uredinospores. The latter were moderately echinulate, light yellow, broadly ellipsoid (length = 23 ± 4 μm and range = 11 to 33 μm; width = 15 ± 2 μm and range = 9 to 20 μm) with walls of 1 to 2 μm thick (mean 1.3 ± 0.2 μm). Hair-like columnar telia (length = 1123 ± 131 μm and range = 976 to 1280 μm; width = 136 ± 28 μm and range = 104 to 176 μm) were mostly formed from uredinia. Telia were hypophyllous and reddish orange. Teliospores were orange-yellow and ellipsoidal to cylindrical (length 26.3 ± 6.2 μm and range 13.5 to 46 μm; width = 10.5 ± 1.8 μm and range = 6.9 to 14.9 μm). Morphological features of these fruiting structures were consistent with those of C. flaccidum (Alb. & Schwein.) G. Winter on white swallow-worts (2). Additional confirmation was provided by sequencing the two internal transcribed spacer regions (ITS1 and ITS2) and the 5.8S gene (4). The sequence was 843 bp long (GenBank Accession No. JN802139), 99.7% similar to C. flaccidum found on Melampyrum in Finland (Accession No. JF13709), and 99.4% similar to C. flaccidum found on pines in Italy (Accession No. X83900). Voucher material has been deposited at the Herbarium of Montpellier's University under the collection Accession No. MPUØ188846. To our knowledge, this is the first report of the occurrence of uredinia and telia of C. flaccidum on black swallow-worts clearly identified in France. The occurrence of the rust on this understory vine is of critical importance for the economic sustainability of pine forests in France, especially when they are heavily constrained by drought and fire.