Fungi infecting woody plants: emerging frontiers.

Trees in natural forests and those managed in plantations of either native or non-native species are increasingly threatened by fungal diseases (Roy et al. 2014, Wingfield et al. 2015, Ghelardini et al. 2017). Typically, the field of forest pathology focuses on this topic. But ironically, it often fails to consider trees outside the classical forestry system. For example, it is unusual for forest pathologists to study diseases of fruit trees, even though these trees originate from natural forests. And their disease threats are closely linked to pathogens that have evolved with the trees where they are native (Burgess & Wingfield 2016, Mehl et al. 2017). There is also increasing evidence that trees share pathogens with woody plants that are not considered to be trees. An example here would be pathogens of grapevines where there are numerous latent pathogens such as those in the Botryosphaeriales shared between these plants (Van Niekerk et al. 2004, Yang et al. 2017).

This dedicated volume was planned specifically to accommodate a suite of papers covering fungi that occur on trees but also to include woody plants not typically treated by tree pathologists. Broadly, our intention was to draw attention to the fact that there are many groups of fungi including important pathogens that occur on forest and fruit trees, but also on woody plants not usually considered by plant pathologists working on tree health problems. Nine papers have been included in this volume that treat a range of pathogen groups including ascomycetes, basidiomycetes and oomycetes. For many of these organisms, Koch’s postulates have been tested and pathogenicity has been confirmed. For others, these tests have yet to be undertaken and some are most likely not pathogens.

The genus Fusarium includes many important plant pathogens or secondary invaders. These fungi have been included in the top 10 globally most important genera of plant pathogenic fungi, based on perceived scientific and economic importance (Dean et al. 2012). Citrus is one of the most important fruit crops worldwide, second only to apple. Neocosmospora (Fusarium) solani s.lat. is the causal organism of a disease known as dry rot of Citrus. In a survey to identify fungal pathogens associated with Citrus in Europe, several fusarium-like isolates were obtained from diverse symptomatic tissues. A total of 11 species (six Fusarium spp. and five Neocosmospora spp.) were isolated from dry root rot, crown, trunk or twig canker or twig dieback. The isolates included three new Fusarium species that are described in the paper by Sandoval-Denis et al. 2018). They include species in the newly described F. citricola species complex; and F. siculi that is in the F. fujikuroi species complex.

Species of Phaeoacremonium are associated with diseases occurring in woody plant tissues. The best-known of these include Petri and esca diseases of grapevines (Crous et al. 1996, Mostert et al. 2006) and dieback and cankers on other fruit trees and woody plants (Gramaje et al. 2015). Several species of woody plants growing in the proximity of vineyards or fruit tree orchards have been shown to harbour species of Phaeoacremonium. In a survey of more than 29 different woody plants growing in close proximity to vineyards in South Africa, 31 species were identified, including 13 novel species (Spies et al. 2018).

The Botryosphaeriaceae includes a wide assemblage of fungi that are associated with dieback and canker diseases of woody plants including both economically important crops and native trees (Slippers & Wingfield 2007, Phillips et al. 2013, Yang et al. 2017). Species of Eucalyptus are amongst the most widely planted trees to sustain plantation forestry globally. There are many examples where these trees are seriously damaged by species of Botryosphaeriaceae including by diseases such as stem cankers, shoot and twig blight. Following an extensive survey of Eucalyptus and adjacent plants in six provinces of China, 12 species of Botryosphaeriaceae were identified, including six new species, of which the Lasiodiplodia species were the most aggressive in pathogenicity tests (Li et al. 2018).

The genus Seiridium includes several important plant pathogenic species, three (S. cardinale, S. cupressi and S. unicorne) of which are involved in the disease of Cupressus spp. known as cypress canker (Graniti 1998, Barnes et al. 2001). Based on a morphological and phylogenetic study, Bonthond et al. (2018) have re-evaluated the taxonomy of Seiridium. Both S. cardinale and S. unicorne are redescribed, with a reference strain designated for each. Authentic material of S. cupressi was re-examined, a lecto- and epitype designated and two new species described. This study resolves a longstanding confusion surrounding the taxonomy of S. cupressi, which is one of the most important pathogens of Cupressus, having a wide global distribution (Graniti 1998).

Species in the Diaporthales (Sordariomycetes) are responsible for several diseases of trees that can result in severe damage (Marin-Felix et al. 2017). The classification of Diaporthales has changed drastically in recent decades, largely due to the plasticity and variability in morphological characteristics that have been applied to their taxonomy. Based on a multigene phylogeny, Fan et al. (2018) have defined 25 families in Diaporthales. Four of these families are associated with canker and dieback of tree hosts are treated in this study. These include three new families (Diaporthostomataceae, Pseudomelanconidaceae, Synnemasporellaceae), and one new genus, Dendrostoma (Erythrogloeaceae). The Diaporthaceae includes several genera (Senanayake et al. 2017), of which Diaporthe is well-known as the causal agent of many important plant diseases, including fruit rots, dieback and stem cankers (Gomes et al. 2013).

Diaporthe species are commonly found associated with major diseases of grapevines (Mostert et al. 2001). Several of these species remain unidentified and have in the past been treated as phylogenetic taxa (Van Niekerk et al. 2005). Very few studies have dealt with the distribution of Diaporthe spp. on grapevine in Europe and other countries from the Mediterranean basin. Guarnaccia et al. (2018) conducted surveys in European countries giving rise to 175 Diaporthe isolates. These included various well-known and four new species. Inoculation tests were conducted to define the relative importance of these fungi.

Diseases caused by species of Ceratocystis as recently defined in the Ceratocystidaceae by De Beer et al. (2014) include vascular wilts, cankers, as well as rot of various root crops (Roux & Wingfield 2009). In recent years, there has been a worrying increase in newly emerging tree diseases caused by Ceratocystis spp. (Ploetz et al. 2013, Tsopelas et al. 2017). In this volume, Barnes et al. (2018) describe a new disease that is rapidly assuming crisis status in Hawai’i and that has colloquially been termed Rapid ‘ôhi’a death (ROD). The disease has resulted in the death of hundreds of thousands of native Metrosideros polymorpha trees on the Big Island of Hawai’i (Mortenson et al. 2016). The pathogen responsible for the wilt symptoms was tentatively identified as C. fimbriata s.lat., and the disease was referred to as Ceratocystis wilt (Keith et al. 2015). However, results of a morphological and phylogenetic study by Barnes et al. (2018) have shown that two new Ceratocystis species, C. lukuohia and C. huliohia, are associated with ROD. Morphology and interfertility tests support the delineation of these new species and pathogenicity tests have shown that both taxa are pathogens although their relative importance has yet to be determined. Attempts are currently underway to prevent the spread of these two pathogens to the other islands of Hawai`i, which are currently disease free.

The oomycete genus Phytophthora includes many species that have a hemibiotrophic or necrotrophic lifestyle as primary plant pathogens, although many aquatic Phytophthora species appear to be saprophytes and opportunistic necrotrophic pathogens (Erwin & Ribeiro 1996, Nechwatal et al. 2013). Several Phytophthora species have both soil- and airborne life-cycles, causing root and collar rot on agricultural crops, and foliage and shoot blights tree hosts. Globally, it has been estimated that up to 66 % of all fine root diseases and more than 90 % of all collar rots of woody plants are caused by Phytophthora species (Tsao 1990). In 1996, only 50 Phytophthora species had been described (Erwin & Ribeiro 1996). Importantly, more than 100 new Phytophthora species have been described in the past two decades (Burgess et al. 2018). The review by Jung et al. (2018) in this volume provides new insights into the history, distribution, symptomatology, disease dynamics and impact of the most important canker, decline and dieback diseases caused by soil- and airborne Phytophthora species in Europe, Australia and the Americas.

The rust fungus Uromycladium tepperianum has been reported on more than 100 species of Acacia, as well as on closely related plant genera. More significantly, it has also been introduced into countries as an important biological control agent to reduce the impact of invasive weeds, such as Acacia saligna in South Africa (Wood & Morris 2007). Based on a phylogenetic study, Doungsa-ard et al. (2018) revealed that U. tepperianum represents a species complex, and described the new species U. morrisii to accommodate the biocontrol agent introduced into South Africa. The authors describe 16 new species based on host range, morphology and phylogenetic data. They also make the important point that additional species of Uromycladium are likely to be discovered when more taxa are examined incorporating DNA data together with their morphology and biology. Their findings also underpin some of the potential consequences of introducing biocontrol agents prior to resolving their taxonomy, and using contemporary molecular techniques that can reveal cryptic taxa.

Papers in this volume raise important issues relevant to the health of trees and other woody plants that might share common pathogens or groups of pathogens. The global movement of plants and plant products is clearly leading to often devastating introductions of new plant pathogens into areas where they were previously not present. In many cases, these pathogens are introduced in the asymptomatic tissues of plants traded for nursery purposes or even as fruit (Crous et al. 2015, 2016). There are huge numbers of these fungi and other microbes, mostly undescribed and often unculturable forming part of the microbiomes of plants as has recently been shown for Eucalyptus by Kemler et al. (2013). Detecting these organisms has relied on microscopy in the past but in future will lean increasingly heavily on molecular techniques for quarantine and screening (McTaggart et al. 2016, Guarnaccia et al. 2017). As illustrated in the papers included in this volume, there is considerable common ground between mycologists working on woody plants inclusive of those pertinent to forestry and fruit farming. In this regard, there is cause to promote closer collaboration between mycologists and plant pathologists with specific interests in horticulture and forestry.