Critical factors driving aphanomyces damping‐off and root disease in clover revealed and explained using linear and generalized linear models and boosted regression trees

Abstract

Subterranean clover (Trifolium subterraneum) is an important forage legume in Mediterranean regions worldwide. Aphanomyces damping‐off and root disease (Aphanomyces trifolii) poses significant threat to its persistence and productivity. Studies were conducted to define how environmental explanatory variables (temperature, soil type, moisture, nutrition) and variety influence disease severity and consequent forage productivity and persistence. Relationships were modelled using linear and generalized linear models and boosted regression trees. Linear modelling highlighted complex relationships between environmental variables and each dependent variable (emergence, tap and lateral root disease, dry shoot and root weight). All environmental variables produced significant interaction and/or main effects within each dependent variable. Boosted regression trees supported the complex nature of relationships in linear models, with temperature and either soil or variety most, and nutrition least, influential. Heat maps showed more disease for low temperatures. Least tap root disease was under high temperatures, while least lateral root disease was under medium or high temperatures, low moisture, and in sand‐based soil. These are the first studies using modelling approaches to reveal the complexities of how fluctuating soil temperature, moisture and nutrition conditions, and soil type and variety, determine aphanomyces damping‐off and root disease severity and resultant adverse impacts on forage legume productivity and persistence. Outcomes are widely applicable across soilborne oomycete pathogens of forage legumes. Studies highlighted how warming temperatures and drying climate associated with climate change should reduce future impact and importance of this and other soilborne oomycete diseases of forage legumes favoured by cold temperatures and wet and waterlogged conditions.

Plant genotype and temperature impact simultaneous biotic and abiotic stress‐related gene expression in Pythium‐infected plants

“…It also showed that RGERs of tested genes and their relationships differed across varieties, temperatures, and infection duration (ID). This was not unexpected, as earlier studies on the interactions between environmental factors on Pythium , Phytophthora , Aphanomyces , and Rhizoctonia root disease severities in different varieties of subterranean clover illustrated the complexity of biotic and abiotic stress combinations phenotypically (e.g., You and Barbetti, ; ; You et al , ; ). The current study provides the first understanding of the connections between phenotypic and gene expressions for subterranean clover infected by P. irregulare , and should lay a foundation for studies of other soilborne oomycete pathogens on subterranean clover and other annual forage legumes.…”

“…Varieties of different resistance/susceptibility show significant differences at both phenotypic and molecular levels when confronted by pathogens (e.g., Ma et al , ; Cregeen et al , ; Kumari et al , ; Tran et al , ). In the current study, while total RGERs were significantly up‐regulated in all tested varieties, it is noteworthy that up‐regulation in moderately resistant Riverina (Nichols et al , ; You et al , ) was significantly different from Seaton Park (susceptible) and Woogenellup (moderately susceptible) at moderate–high temperatures, confirming that genotype is a critical factor that not only affects gene transcripts but also affects the expression of phenotypic characteristics such as root disease, plant size, and growth rate (You and Barbetti, ; ; You et al , ; ).…”

“…Furthermore, there has been little if any work done on abiotic stress resistance in subterranean clover, and none that the authors are aware of in relation to the expression of abiotic defence‐related genes. Studies on the interactions between environmental factors and severities of Pythium , Phytophthora , Aphanomyces , and Rhizoctonia root disease in different varieties of subterranean clover not only illustrated the phenotypic effects of the complex biotic and abiotic stress combinations (You and Barbetti, ; ; You et al , ; ), but also unwittingly highlighted the lack of understanding of the “connections” between phenotypic and gene expression for these pathogens/diseases of forage legumes. Importantly, there are no previous studies that compare and contrast gene expression in response to abiotic and biotic stress in subterranean clover.…”

Manipulating the ecosystem enables management of soilborne pathogen complexes in annual legume forage systems

“…For example, where annual forage legumes are severely affected by root disease, there can be a wide range and variability for plant and disease symptoms across locations and seasons (Barbetti et al ., , ), as symptoms are strongly influenced by environmental factors (e.g. You & Barbetti, ,b; You et al ., , ). That DNA weights were lower in 100% than 20% clover composition across all tested varieties, further explains observations noted above that as clover forage stands become adversely affected by oomycete soilborne pathogens, the severity of root disease and the rate of stand decline both increase dramatically (authors’ unpublished data).…”

“…The soilborne pathogens of clovers occur as a pathogen complex and the most important include the oomycete pathogens Pythium irregulare , Phytophthora clandestina , Aphanomyces trifolii and the fungal pathogens Rhizoctonia solani and Fusarium avenaceum (Barbetti & MacNish, ; Taylor et al ., ; Wong et al ., ,b; Barbetti et al ., ; You et al ., , ; O'Rourke et al ., ; Nichols et al ., ; You & Barbetti, ,b). While P. clandestina and A. trifolii seem relatively specialized to clovers (You et al ., , ; O'Rourke et al ., ; You & Barbetti, ,b), P. irregulare is almost universally present across diverse hosts including a range of different forage legumes (Hendrix & Campbell, ). For example, P. irregulare is a seedling damping‐off and root rot pathogen regarded as the most frequent and widespread pathogen responsible for extensive pre‐emergence damping‐off and severe root disease in clovers across southern Australia over the past four decades (Stovold, ; Barbetti & MacNish, ; Greenhalgh & Lucas, ; Wong et al ., ; Barbetti et al ., ; Nichols et al ., ).…”