Indirect Evidence Based on Mating-Type Ratios for the Role of Sexual Reproduction in European and Chinese Populations of Plenodomus biglobosus (Blackleg of Oilseed Rape)

Blackleg (Phoma) disease, caused by the ascomycete fungi Plenodomus biglobosus and P. lingam, threatens oilseed rape (OSR; Brassica napus) crops internationally. In many parts of the world, both species co-occur, but in China only P. biglobosus has so far been reported. Plenodomus biglobosus reproduces asexually (pycnidiospores), but also sexually (pseudothecia-yielding ascospores), via a heterothallic mating system requiring MAT1-1 and MAT1-2 genotypes. However, the roles of airborne ascospore inoculum in driving blackleg disease outbreaks in China are less well understood compared to elsewhere in the world. This is despite the very different agronomic cropping practices in parts of China, in which paddy rice and OSR are often grown in rotation; OSR stubble is often submerged under water for long periods potentially affecting pseudothecial development. Here, we indirectly investigate the potential role of sexual reproduction by developing new polymerase chain reaction (PCR) -based mating-type diagnostics for P. biglobosus and subsequently screening an international collection of 59 European and 157 Chinese isolates. Overall, in both Europe and China, P. biglobosus mating types did not deviate from a 1:1 ratio, such as is generally thought to occur under frequency-dependent selection in sexually reproducing pathogen populations. Both mating types were balanced in all the individual European countries tested (Austria, France, Poland, UK). Conversely, in China, mating types were only balanced in the eastern region; in the northern and southwestern regions there were skewed ratios, more typical of predominantly asexual reproduction, towards MAT1-1 and MAT1-2, respectively. The implications of these findings and future research directions for improved understanding of P. biglobosus epidemiology on OSR, particularly in China, are considered.

[1]  A. Dolatabadian,et al.  Genetic structure and phylogenetic relationships of Leptosphaeria maculans and L. biglobosa in Northern regions of Iran , 2022, Archives of Phytopathology and Plant Protection.

[2]  J. West,et al.  Detection of the Phoma pathogens Plenodomus biglobosus subclades ‘brassicae’ and ‘canadensis’ on wasabi, and ‘canadensis’ in Europe , 2021, European Journal of Plant Pathology.

[3]  Mehdi Mehrabi-Koushki,et al.  Plenodomus dezfulensis sp. nov. causing leaf spot of Rapeseed in Iran , 2021, Phytotaxa.

[4]  A. P. Van de Wouw,et al.  A New Subclade of Leptosphaeria biglobosa Identified from Brassica rapa , 2019, International journal of molecular sciences.

[5]  P. Wincker,et al.  De novo assembly and annotation of three Leptosphaeria genomes using Oxford Nanopore MinION sequencing , 2018, Scientific Data.

[6]  W. Fernando,et al.  Insights into fighting against blackleg disease of Brassica napus in Canada , 2018, Crop and Pasture Science.

[7]  G. Rodríguez,et al.  Phoma leaf spot of wasabi (Wasabia japonica) caused by Leptosphaeria biglobosa , 2017 .

[8]  Li-min Hao,et al.  Genetic diversity and differentiation of Leptosphaeria biglobosa on oilseed rape in China , 2015, Phytoparasitica.

[9]  B. Fitt,et al.  Importance of Leptosphaeria biglobosa as a cause of phoma stem canker on winter oilseed rape in the UK , 2014 .

[10]  B. Fitt,et al.  Phoma stem canker disease on oilseed rape (Brassica napus) in China is caused by Leptosphaeria biglobosa ‘brassicae’ , 2014, European Journal of Plant Pathology.

[11]  Robin P. White,et al.  Leptosphaeria spp., phoma stem canker and potential spread of L. maculans on oilseed rape crops in China , 2014 .

[12]  T. Rouxel,et al.  Clonal populations of Leptosphaeria maculans contaminating cabbage in Mexico , 2013 .

[13]  P. Crous,et al.  Redisposition of phoma-like anamorphs in Pleosporales , 2012, Studies in mycology.

[14]  M. Jędryczka,et al.  Quantitative PCR analysis of abundance of airborne propagules of Leptosphaeria species in air samples from different regions of Poland , 2012, Aerobiologia.

[15]  T. Giraud,et al.  Migration patterns and changes in population biology associated with the worldwide spread of the oilseed rape pathogen Leptosphaeria maculans , 2012, Molecular ecology.

[16]  M. Jędryczka,et al.  The effect of winter weather conditions on the ability of pseudothecia of Leptosphaeria maculans and L. biglobosa to release ascospores , 2012, European Journal of Plant Pathology.

[17]  B. Marchant,et al.  Geostatistical analysis of the distribution of Leptosphaeria species causing phoma stem canker on winter oilseed rape (Brassica napus) in England , 2010 .

[18]  B. Fitt,et al.  Strategies to prevent spread of Leptosphaeria maculans (phoma stem canker) onto oilseed rape crops in China; costs and benefits , 2008 .

[19]  Hua Li,et al.  Occurrence of a new subclade of Leptosphaeria biglobosa in Western Australia. , 2008, Phytopathology.

[20]  T. Rouxel,et al.  Genetic Variability and Distribution of Mating Type Alleles in Field Populations of Leptosphaeria maculans from France , 2006, Applied and Environmental Microbiology.

[21]  J. M. Steed,et al.  Patterns of ascospore release in relation to phoma stem canker epidemiology in England (Leptosphaeria maculans) and Poland (Leptosphaeria biglobosa) , 2005, European Journal of Plant Pathology.

[22]  B. Howlett,et al.  Genetic diversity of Australian isolates of Leptosphaeria maculans, the fungus that causes blackleg of canola (Brassica napus) , 2004, Australasian Plant Pathology.

[23]  T. Rouxel,et al.  Molecular phylogeny of the Leptosphaeria maculans-L. biglobosa species complex. , 2003, Mycological research.

[24]  A. Cozijnsen,et al.  Characterisation of the mating-type locus of the plant pathogenic ascomycete Leptosphaeria maculans , 2003, Current Genetics.

[25]  J. M. Steed,et al.  Colonization of winter oilseed rape tissues by A/Tox+ and B/Tox0 Leptosphaeria maculans (phoma stem canker) in France and England , 2002 .

[26]  Bruce D.L. Fitt,et al.  Epidemiology and management of Leptosphaeria maculans (phoma stem canker) on oilseed rape in Australia, Canada and Europe , 2001 .

[27]  J. West,et al.  Leptosphaeria maculans causing stem canker of oilseed rape in China , 2000 .

[28]  S. Lob Leptosphaeria diseases of oilseed rape and swede: identification and epidemiology , 2014 .

[29]  Rong Song-bai,et al.  Distribution of blackleg disease on oilseed rape in China and its pathogen identification , 2013 .

[30]  M. Barbetti,et al.  World-Wide Importance of Phoma Stem Canker (Leptosphaeria maculans and L. biglobosa) on Oilseed Rape (Brassica napus) , 2005, European Journal of Plant Pathology.

[31]  B. McDonald,et al.  Pathogen population genetics, evolutionary potential, and durable resistance. , 2002, Annual review of phytopathology.