Botryosphaeriaceae on Syzygium cordatum across a latitudinal gradient in South Africa

Highlights

• Fourteen Botryosphaeriaceae species were isolated from Syzygium cordatum (Waterberry).

• Maximum historical temperature influenced community composition of Botryosphaeriaceae species.

• Botryosphaeriaceae species richness was not influenced by maximum historical temperature.

• Optimal growth temperature of all Botryosphaeriaceae isolates in culture was 25 °C.

• The origin of the samples was not related to the growth temperature of the isolates.

Abstract

The Botryosphaeriaceae is a family of endophytic fungi, many of which are latent pathogens of woody plants. Although extensively sampled in some parts of the world, little is known regarding their occurrence across different environmental conditions. This study considered the presence of the Botryosphaeriaceae on Syzygium cordatum trees across a latitudinal gradient. We examined the relative importance of different environmental factors on the presence of the Botryosphaeriaceae across this latitudinal gradient. Specifically, Botryosphaeriaceae community composition and species richness were analysed. The optimal growth temperature of the most common Botryosphaeriaceae isolates and its relation to isolate origin was also tested in culture. We identified 14 Botryosphaeriaceae species including seven each of Lasiodiplodia and Neofusicoccum species. The maximum historical temperature emerged as the environmental factor that best predicted the presence of Botryosphaeriaceae species in S. cordatum trees, specifically influencing Botryosphaeriaceae community composition. For all the Botryosphaeriaceae species studied in vitro, temperature strongly influenced mycelial growth and they all had an optimal growth temperature of 25 °C. Contrary to our hypothesis, the optimal growth temperature was not related to isolate origin. These results contribute to understanding the presence of the Botryosphaeriaceae in trees and our ability to detect these latent pathogens.

Introduction

The Botryosphaeriaceae is a taxonomically diverse family of endophytic fungi with a broad host plant range and wide geographic distribution. The family accommodates 23 genera including important pathogens such as species of Botryosphaeria, Diplodia, Dothiorella, Macrophomina and Neofusicoccum. All the genera have been delineated based on comparisons of DNA sequence data in combination with morphological characters (Crous et al., 2015; Phillips et al., 2013; Slippers et al., 2017).

The Botryosphaeriaceae are common on commercially cultivated and native tree species (Mehl et al., 2013; Slippers and Wingfield, 2007). Many of these fungi are latent and opportunistic plant pathogens, predominantly of woody plants (Mehl et al., 2013; Slippers and Wingfield, 2007). They infect trees via wounds or natural openings, causing disease when their hosts are stressed (Slippers and Wingfield, 2007). Diseases attributed to these fungi span all the life stages of plants including seedling damping-off and blight, stem and branch cankers and die-back, blue-stain, root rot, fruit rots, seed capsule abortion, and death of mature trees (Slippers and Wingfield, 2007).

The damage caused by pathogenic Botryosphaeriaceae has stimulated surveys for these fungi, mainly focused on commercially cultivated plants (Bihon et al., 2012; Chen et al., 2011; Trakunyingcharoen et al., 2014; Úrbez-Torres, 2011). However, these studies have not considered how abiotic variables could affect the Botryosphaeriaceae. Recently, Burgess et al. (2019) published a study examining the distribution (location and climate) and host range of these taxa in Australia. This is an important knowelege gap because environmental variables can influence fungal endophyte community composition and diversity in plant species (Coince et al., 2014; Cordier et al., 2012; Giauque and Hawkes, 2016; Peršoh, 2015). For example, tree endophyte composition differs along a gradient of elevation and the variations are correlated with changes in climatic variables in forests dominated by Fagus sylvatica (Coince et al., 2014; Cordier et al., 2012). Similarly, endophyte diversity decreases from cooler and wetter sites to warmer and drier sites in Panicum hallii (Giauque and Hawkes, 2016). Especially for the Botryosphaeriaceae, temperature is known to influence the life-cycles of these fungi, hindering or promoting spore production (Swart and Wingfleld, 1991). Consequently, environmental variables are expected to influence species presence of these fungi in natural environments.

The Botryosphaeriaceae have been extensively sampled in Syzygium cordatum, a species of Myrtaceae native to South Africa (Pavlic et al, 2004, 2007, 2009; Pavlic-Zupanc et al., 2015; Pillay et al., 2013). These studies have been prompted due to the relatedness of S. cordatum to Eucalyptus that are planted commercially in the country. Importantly, nothing is known regarding the influence of environmental variables on the presence of Botryosphaeriaceae on this tree.

S. cordatum occurs along a latitudinal gradient on the east coast of South Africa (Palgrave, 2002). Its distribution stretches from warm sub-tropical areas in the north to cooler temperate areas in the south. Trees grow in close proximity to plantations of commercially propagated non-native Eucalyptus species (Myrtaceae) that are known to be alternative hosts for several groups of important pathogens such as the Cryphonectriaceae (Mausse-Sitoe et al., 2016) but also for the Botryosphaeriaceae (Pavlic et al., 2007). Consequently, S. cordatum provides a unique opportunity for a case study to interrogate and understand the presence of the Botryosphaeriaceae across a latitudinal gradient.

The objectives of this study were to: i) identify the species of Botryosphaeriaceae present on S. cordatum trees along a latitudinal gradient on the east coast of South Africa, ii) consider the possible effect of different environmental conditions (historical-climate and current-weather) across this gradient on the presence of the Botryosphaeriaceae on these trees, and iii) determine the optimal temperature for in vitro mycelial growth of the collected Botryosphaeriaceae, in order to consider whether this might be related to isolate origin across the latitudinal gradient.