Ganoderma Diseases of Tropical Crops

By Carmel A Pilotti and Paul Dennis Bridge

The fungal genus Ganoderma includes around 80 currently recognized species that are widely distributed in temperate, subtropical and tropical regions, and cause disease in a range of economically important perennial crops and tree-like plants.

Ganoderma root and lower stem rots have a significant impact on yields from crops including oil palm, coconut, beverage crops, Acacia and rubber. The identification of species responsible for stem and butt rots is often ambiguous as closely related species may only be distinguished by subtle morphological differences. Within species there can be considerable morphological plasticity and this can make morphology-based identification difficult, particularly for species described from a single specimen. Molecular techniques are helping to slowly resolve Ganoderma taxonomy but it will be some time (if ever) before the taxonomy is fully resolved.

This book brings together information on Ganoderma species that are reported to be responsible for crop diseases in tropical and sub-tropical agriculture and covers taxonomy, biology, genetics, aetiology, epidemiology and control. This book is an essential resource for researchers in Ganoderma in crop science and tropical agriculture, as well as practitioners and industry.

• Language: English
• Publisher: CAB International
• Release date: Nov 28, 2023
• ISBN: 9781800620780

Carmel A Pilotti

Dr Carmel A. Pilotti has been involved with research on Ganoderma species on oil palm, particularly G. boninense for c. 25 years. Prior to attachments in agriculture she worked in the forestry sector in Papua New Guinea in the areas of phytochemistry and fungal decay of timber. She is currently working on the genetic diversity of coconut (Cocos nucifera) and is employed by the Pacific Community at the Centre for Pacific Crops and Trees (CePaCT).

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Ganoderma Diseases of Tropical Crops

Ganoderma Diseases of Tropical Crops

by

Carmel A. Pilotti

and

Paul D. Bridge

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A catalogue record for this book is available from the British Library, London, UK.

ISBN-13:9781800620766 (hardback)

9781800620773 (ePDF)

9781800620780 (ePub)

DOI: 10.1079/9781800620780.0000

Commissioning Editor: Rebecca Stubbs

Editorial Assistant: Lauren Davies

Production Editor: Shankari Wilford

Typeset by SPi, Pondicherry, India

Printed and bound in the UK by Severn, Gloucester

Contents

Preface

1Introduction

2Taxonomy

3Biology and Genetics

4Disease Detection

5Oil Palm

6Coconut Palm

7Other Palms and Other Monocotyledon Hosts

8Acacia Species

9Beverage Crops (Tea, Cocoa and Coffee)

10 Rubber

11 Other Tropical Crops Affected by Ganoderma Species

12 Major Pathogens of Palms

13 Pathogens of Woody Crops

14 Other Species Reported Pathogenic to Tropical Commodity Trees

15 Common Issues for Improved Management of Ganoderma Diseases

Appendix 1. Sequences used for phylogenetic analyses in Figs 2.1, 12.1, 13.1 and 14.1

Appendix 2. Details of herbaria referenced in Chapters 12–14

References

Index

Preface

The genus Ganoderma has long been associated with root and lower-stem rots in tropical perennial crops. Although a number of species of Ganoderma have been associated with different crops, the symptoms on the plant are broadly similar and frequently do not become apparent before extensive infection has occurred, often developing over a number of years. In many tropical crops disease occurrence is limited to individual or small groups of older trees, and while sanitation methods can be labour intensive, there is often little significant economic loss. Conversely, in some crops such as oil palm, the disease can become established over large areas of plantations and result in considerable financial losses. The fungus appears to then spread to new plantings, resulting in disease occurring earlier in the planting cycle and increasing losses.

The increasing impact of Ganoderma rots on oil palms in South Asia and Oceania, and on coconuts in India, has driven considerable research activity in the regions over the last 30–40 years. In most instances this has been crop specific, but there have been a number of previous attempts to increase research linkages and bring together information from across the broad tropical perennial crop environment. A series of workshops based in Malaysia in 1998 led to publication of the book Ganoderma Diseases of Perennial Crops (CAB International, Wallingford, UK) in 2000 and a subsequent mixed crop workshop in Indonesia in 2003 was published through the journal Mycopathologia (Mycopathologia 159(1)) in 2005. In the 20+ years since those publications, there have been a number of significant developments regarding Ganoderma crop diseases. Some of these developments relate to crops; for example, oil palm basal stem rot has now been reported in Africa and South America (see Chapter 5, this volume) and economic losses from Ganoderma rots have now been reported in other plantation crops including acacias (see Chapters 8 and 11, this volume). Although Ganoderma diseases appear to be an increasing problem, possibly the most significant developments in the last 25 years have been in our understanding of the taxonomy of the genus, and with that, our ability to accurately detect and identify the potential pathogens.

In 1995 Ryvarden described the genus Ganoderma as being ‘in a state of taxonomic chaos’ (see Chapter 2, this volume). Since then the rapid development of molecular techniques for fungal taxonomy and phylogeny has allowed some clarification of the species concepts in the genus. This in turn is now leading to a better understanding of the pathogens involved, their biogeography and their population structures. Further developments such as the digitization of older literature and public depositories for DNA sequence data allow for wider studies and comparisons of the fungi involved in different disease situations.

In this volume we have attempted to bring together the available information to give an overview of the current knowledge of Ganoderma diseases of tropical crops. We have organized this in three sections, with one describing the history and features of the genus (Chapters 1–4), one providing reviews for individual crops (Chapters 5–11) and a third section giving details of particular Ganoderma species associated with one or more perennial crop plants (Chapters 12–14). There are some 400+ species and varieties listed in the genus Ganoderma (see Chapter 2), and for this volume we have focused on the 20–30 species that have been reported as causing economically significant crop losses. We are particularly grateful to the various colleagues and organizations who have allowed us to reproduce photographs and figures to illustrate the text throughout (see figure credits).

In future years it is likely that both taxonomic opinions and agricultural practices will develop further, and it is hoped that this review of the current knowledge will provide some background and insights for the management of Ganoderma root and stem rots in the future.

Carmel A. Pilotti

Paul D. Bridge

1

Introduction

Abstract

The genus Ganoderma includes some of the longest continually studied fungi in human history. Some species have been long established as potential medicinal agents, whereas others have been observed to cause root and stem rots on a variety of tropical and subtropical commodity trees. This chapter provides a brief introduction to the genus and an overview of the commodity trees affected.

History

The basidiomycete genus Ganoderma includes some of the longest documented fungi in the history of human science. Fungi in the genus have been known and studied for at least 2000 years and taxa such as Ganoderma lingzhi have been documented in traditional East Asian medicine under a variety of names including Lingzhi and Reishi since the Eastern Han dynasty (AD 25–220) in China (see Chang, 1995; Seo and Kirk; 2000; Chapter 2, this volume). Individual taxa have long been reported in China and Japan as medicinal herbs and to possess considerable health benefits when ingested (for reviews, see Wachtel-Galor et al., 2011; Lin, 2019). Different taxa were designated on the basis of the colour and shape of the fruiting bodies with red, black, blue, yellow, purple and white forms being described in historic Chinese literature. Some of these can be identified with modern species names such as G. lingzhi (e.g. Cao et al., 2012) and Ganoderma neojaponicum (Jo et al., 2010), whereas the identity of others, particularly the blue, yellow and white forms, remains unknown (see Zhao, 1989; Seo and Kirk, 2000). In addition to their long medicinal history in China and Japan, Ganoderma species have also been used in indigenous preparations throughout Asia and Oceania. One example of this is illustrated by a specimen in the Kew herbarium collected in 1963 and identified by Steyaert as Ganoderma mastoporum (see Fig. 1.1). The herbarium packet is annotated with the comment that ‘the mushroom is not eaten as a food by the natives but eaten by young women as a contraceptive or abortive medicine’.

A photo of a label for Ganoderma mastoporum used in a herbarium.

Fig. 1.1. Annotated herbarium label for a 1963 collection of Ganoderma mastoporum. (Photo by P.D. Bridge.)

As a result of this long medicinal and pharmacological history, the biochemistry of the traditionally utilized species has been extensively studied, with a particular emphasis being placed on identifying compounds with biological and pharmacological activities (see Baby et al., 2015; Chapter 3, this volume). Most analytical biochemistry research activity has focused on identifying compounds with medicinal benefits, but the potential role of metabolites produced by Ganoderma during plant infections is also now receiving some attention (see Shokrollahi et al., 2021; Chapter 3, this volume). In addition, some authors have suggested that the particular classes and types of metabolites produced by different Ganoderma species may be useful in developing an underlying chemotaxonomy for the genus (see Richter et al., 2015; Chapter 2, this volume).

In the modern era, the name Ganoderma was introduced by Karsten in 1881 (Patouillard, 1889). Derived from the Greek terms ganos for ‘shiny’ and derma for ‘leather’ or ‘hide’, it was descriptive of the typical dark brown fruiting bodies produced on woody substrates. As originally described, the genus consisted of the single species Ganoderma lucidum and over the years this has expanded to the current situation where over 400 specific and subspecific names have been described (see Chapter 2, this volume).

Ecology

Fungi of the genus Ganoderma are closely associated with woody plants, where they can be observed as a fruiting body or sporophore in the form of a bracket that forms on the surface of stems, trunk and roots. The genus has been placed in the order Polyporales and the fruiting bodies have numerous pores on the underside from which monokaryotic basidiospores are released. These basidiospores fuse to form dikaryotic mycelium which ultimately gives rise to a new fruiting body (see Chapter 3, this volume). Ganoderma species produce large numbers of spores from their fruiting bodies (see Fig. 1.2 and Chapters 5 and 15, this volume) and can persist and spread in the environment as either basidiospores or through mycelial growth, although the production of fruiting bodies usually only occurs from plant material, or occasionally from soil containing plant debris (see Chapter 3, this volume).

A photo of the fruiting bodies of Ganoderma at the base of the tree trunk.

Fig. 1.2. Ganoderma fruiting bodies showing a large number of liberated basidiospores as brown deposits on the tree trunk and surrounding vegetation. (Photo by P.D. Bridge.)

One of a number of fungal genera collectively known as ‘white-rot fungi’, Ganoderma fungi have the ability to selectively delignify wood, while also utilizing cellulose and polysaccharides (see Adaskaveg and Gilbertson, 1986a; Adaskaveg and Ogawa, 1990; Seo and Kirk, 2000; Chapter 3, this volume). The white-rot fungi are recyclers in nature and commonly occur as saprophytes in the natural environment on forest trees, shrubs and palms. They have strong enzymatic activities, including very active oxidases and peroxidases, in order to break down lignin and other plant material (see Zhou et al., 2013; Chapter 3, this volume).

The genus is considered to be cosmopolitan and species of Ganoderma have been reported worldwide on an enormous range of over 200 species of woody plants and vines, including both dicot and monocot angiosperms and some gymnosperms (for some examples of range, see Steyaert, 1972, 1980; Tan et al., 2015; Hapuarachchi et al., 2018, 2019; Fryssouli et al., 2020; Luangharn et al., 2021). In recent years, as Ganoderma species have become better delineated, there have been a number of investigations into potential biogeographical distributions for certain species (e.g. Moncalvo and Buchanan, 2008; Fryssouli et al., 2020). The genus has been presumed to be less than 30 million years old and so would have diversified after the formation of the major continents, thus other factors such as wind dispersal of spores may be a significant factor in their current distribution (see Moncalvo and Buchanan, 2008; Chapter 2, this volume). Although frequently occurring as saprobes on dead wood, many species are facultative parasites and may spend part of their life cycle as endophytes in living trees before emerging as parasites or pathogens (Martin et al., 2015; Loyd et al., 2018b).

Identification

Although fruiting bodies, spores and cultures of Ganoderma species can include many morphological features, these can be highly variable between individuals and can be difficult to interpret. As a result there has been considerable controversy on the naming of taxa at the species level based on morphology (see Ryvarden, 1995). This is explained in detail in Chapter 2 (this volume) and the situation is slowly being resolved through molecular studies (e.g. Cao et al., 2012; Hapuarachchi et al., 2015; Loyd et al., 2018a; Fryssouli et al., 2020). These molecular studies have been able to differentiate many taxa previously associated with morphological species complexes and to identify new species-level groups (see Chapters 2, 12, 13 and 14, this volume). This increased understanding of the phylogeny of the genus over the last 20 years has led to some significant changes in species concepts and it is important to consider these when considering older reports and literature. It is therefore very difficult to determine the correct current species name for many of the historical records of Ganoderma species in the literature and any new identifications need to be made against recently validated reference material, preferably including DNA sequence data (see Bridge, 2020). The issue of determining correct current names is perhaps less of a problem for some species such as Ganoderma philippii (syn. Ganoderma pseudoferreum) (e.g. Coetzee et al., 2011), but it remains a significant problem with other species, particularly the laccate (shiny) collections that have frequently been assigned to the G. lucidum complex (see Cao et al., 2012; Hapuarachchi et al., 2015; Loyd et al., 2018a; Chapter 2, this volume). Individual crops may be affected by more than one disease caused by Ganoderma, such as Acacia red and yellow root rots (see Irianto et al., 2006; Chapter 8, this volume), and this can also lead to confusion in the species reported. In some cases, such as in basal stem rot in coconuts, there is still no overall consensus as to the correct name for the causal agent (see Rolph et al., 2000; Chapter 6, this volume).

Tropical Crop Diseases

As facultative plant pathogens, some Ganoderma species can cause considerable economically significant losses through stem and root rots in crop plants, particularly in tropical and subtropical ecosystems (see Lee and Chang, 2016). In the subtropical and tropical zones, Ganoderma species occur on numerous woody plants and vines and have historically been reported to cause root and stem rots in many commercial plantings, including in coconuts, tea and rubber (see Chapters 6, 9 and 10, this volume). In recent years Ganoderma diseases have been increasingly reported in newly introduced tree crops, particularly oil palm and Acacia spp., where significant incremental economic losses have been reported (see Chapters 5 and 8, this volume). Ganoderma species have also been reported to cause root and stem rots, although of less economic significance, in a wide range of other important trees and crops including Citrus spp. and other trees grown for fruits and timber (see Chapter 11, this volume). It is difficult to determine the range and significance of Ganoderma root and stem rots in crop plants. In oil palm there are many published studies and scientific reports (see Flood et al., 2022; Chapter 5, this volume), and there are a growing number of such references for diseases in coconut palms and acacias (see Chapters 6 and 8, this volume). However, for most other crops such as tea and rubber, while there are many anecdotal reports, there are comparatively few scientific papers or other published reports linked to verifiable specimens or disease occurrences. It should be noted that Ganoderma species may colonize trees through wounds or other damaged tissues and grow largely saprophytically, and so a report of Ganoderma occurring on a living tree does not necessarily indicate that a root or stem rot was present (see Chapter 14, this volume). Some examples of commercially grown subtropical and tropical trees where Ganoderma species have been reported to cause root and stem rots are given in Table 1.1. This is an extensive, but probably incomplete list as many isolated or very local incidences are unlikely to be widely reported in the literature.

Table 1.1. Examples of commercially significant subtropical and tropical trees and vines where Ganoderma species have been reported to cause economic or significant losses. For a full range of Ganoderma species reported, see Table 14.1 (this volume).

One important feature of Ganoderma diseases in tropical crops is their progressive nature. It has been suggested for some crops such as oil palm and Acacia spp. that initial infections may be due to basidiospores coming from surrounding vegetation, or from mycelial growth from isolated debris in the soil (e.g. Thompson, 1931; Irianto et al., 2006; Pilotti et al., 2018; Chapters 5 and 8, this volume). The presence of the infected plants then provides an increased inoculum potential in the local environment as the trees grow. As a result, infection levels may increase with time and the subsequent disruption and debris can increase disease risks at replanting (see Flood et al., 2005, 2022; Mohammed et al., 2014). This is particularly apparent from the increasing levels of infection (and losses) observed with the increasing age of trees, and the increased levels of infection frequently seen in subsequent crops after replanting (see Rishbeth, 1955; Ariffin et al., 2000; Irianto et al., 2006; Mohammed et al., 2014; Chakruno et al., 2022; Chapters 5 and 8, this volume). In tea cultivation, fallow periods of up to 2 years have been recommended before replanting (see Lehmann-Danzinger, 2000; Chakruno et al., 2022; Chapter 9, this volume). It may therefore be necessary to consider previous vegetation prior to planting. Turner (1965a) found that oil palms planted into old coconut stands showed higher levels of disease than palms planted into old rubber-growing areas, and more recently the possibility of Ganoderma disease being introduced by debris from previous forest trees has been considered for plantings of Acacia and Eucalyptus species (Masuka and Nyoka, 1995; Mohammed et al., 2006; Beadle et al., 2012; Page et al., 2020). Fox (1977) showed that complete mechanical clearing of previous materials resulted in lower subsequent disease levels in rubber in comparison to tree and stump poisoning methods. ‘Complete clearing’ remains the most widely recommended method for minimizing disease risk at planting for other affected crops (see Hasan and Turner, 1998; Ariffin et al., 2000; Mohammed et al., 2014). It has been suggested that the relatively short growing periods of some trees (e.g. in Eucalyptus spp.) may minimize the risk of Ganoderma diseases (see Old et al., 2003).

It is difficult to determine precise figures for crop losses due to Ganoderma diseases. In rubber, red root due to Ganoderma has been reported worldwide (e.g. Rao and Bezerra, 1980; Nandris et al., 1987; Johnston, 1989; He et al., 2019), but is particularly prevalent in South-East Asia (see Wastie, 1975; Mohammed et al., 2014). Fox (1977) reported a 25% loss in rubber yield in areas where red root was prevalent but developed potential loss models on the basis of all root rots. Similarly, other loss models have focused on ‘all’ root rots and so it is difficult to determine the impact of only Ganoderma rots. Ganoderma root rots of tea have been reported from most tea-growing areas, but with widely differing levels of severity (e.g. Agnihothrudu, 1969; Varghese and Chew, 1973; Bauer, 1998; Lehmann-Danzinger, 2000; Sarkar and Kabir, 2016). In most instances crop losses are frequently reported for a single, or group, of plantations, and there seem to be relatively few studies that have attempted to estimate losses at a national or regional level. The exceptions to this are possibly the more recently expanded crops such as oil palm and Acacia where losses of over 20% of trees have been reported for both crops, although in some instances losses can increase to 80% after successive replantings (see Roslan and Idris, 2012; Bhadra, 2014; Mohammed et al., 2014; Flood et al., 2022). In oil palm there has been some modelling of projected loss figures (e.g. Kamu et al., 2021) and it has been reported that in Malaysia alone some 60 million mature oil palms could be infected (see Fernanda et al., 2021).

The importance of Ganoderma diseases of perennial crops in the tropics has probably not been fully realized due to the scarcity of historical information for some crops and the conflicting information on the identities of the causal agents. As modern methods of classification are applied to new and existing diseases, resolution of species identities and corresponding disease aetiologies will no doubt reveal the true impact of stem and root rots caused by fungi in this genus.

2

Taxonomy

Abstract

This chapter provides some basic background into the classification and identification of Ganoderma species. This includes consideration of possible biogeographic species distribution. The chapter contains information on the major morphological characteristics that have been used to delineate taxa in the genus and summarizes the use of physiological and chemical methods in their taxonomy. Current molecular and phylogenetic approaches are considered, and a simplified phylogeny of the main plant pathogenic species is provided.

Introduction

Despite some 2000 years of continuous study, many aspects of Ganoderma taxonomy remain unclear. The genus Ganoderma was first described by Karsten (1881) and then revised by Patouillard (1889). In the subsequent 130 years numerous authors have added species and suggested further generic and subgeneric groupings. Some aspects of these remain unresolved and in 1995 Ryvarden described the genus as ‘currently in a state of taxonomic chaos’ (Ryvarden, 1995).

The Genus

The position of the genus within the Basidiomycota has historically been uncertain. Donk (1948) proposed that the genus Ganoderma and the sister genus Elfvingia (see below) should be grouped in a single family, the Ganodermataceae. Subsequent molecular studies have not supported this separation and current thinking places Ganoderma (including species from Elfvingia) as a distinct genus in the family Polyporaceae (see Binder et al., 2013; Justo et al., 2017; reviewed in Papp, 2019). The detailed history of the genus has recently been described in depth by various authors (e.g. Seo and Kirk, 2000; Hapuarachchi et al., 2019; Papp, 2019).

Subgeneric Groups

The genus Ganoderma as proposed by Karsten in 1881 consisted of a single UK species, Ganoderma lucidum, previously named as Polyporus lucidus by Curtis (Seo and Kirk, 2000). Karsten’s original description included the term ‘laccate’ (shiny) and subsequently Karsten proposed the genus Elfvingia, based on Elfvingia applanatum, for similar fungi with double-walled spores but dull or matt fruiting bodies (Karsten, 1889). Subsequently the non-laccate species were considered to belong to a subgenus within Ganoderma and so were named as Ganoderma species (see Steyaert, 1980; Buchanan and Wilkie, 1995). However, macroscopic features of fruiting bodies can be dependent on the host and environmental conditions (see Ryvarden, 1995) and subsequent molecular studies have shown that a laccate or non-laccate appearance can be affected by the age of the fruiting body, while some species have been described as ‘weakly laccate’ (e.g. Wang et al., 2014; Hapuarachchi et al., 2019). In recent molecular phylogenies species traditionally accepted as non-laccate have been recovered in at least two separate groups, sometimes also containing laccate species (Moncalvo, 2000; Hapuarachchi et al., 2019; Fryssouli et al., 2020), and so there is some doubt as to the taxonomic usefulness of this characteristic, especially where only single specimens are examined. This is discussed in further detail in the ‘Morphology’ subsection below.

One alternative to the use of subgenera is to consider species and species groups that are recovered together in distinct arms or ‘clades’ in phylogenetic analyses. This has been undertaken on a number of occasions and Table 2.1 provides a brief comparison of some of the key species grouped in some of the distinct clades recovered by Moncalvo (2000) and Fryssouli et al. (2020) in two genus-wide phylogenetic studies. Although there are large differences in the number of species considered between these studies, and they were conducted 20 years apart, there is considerable congruence between the major groupings that were suggested in the two studies. Figure 2.1 shows these groupings in a simplified phylogenetic treatment of ribosomal DNA (rDNA) internal transcribed spacer (ITS) sequences for some of the species of particular interest in plant pathology.

Table 2.1. Equivalent subgeneric ITS groups in Ganoderma.

a Species not included in Moncalvo (2000).

A chart of the evolution tree with bootstrap values with group designations of the Ganoderma species.

Fig. 2.1. Rooted minimum evolution tree for ITS sequences of species of Ganoderma reported as plant pathogens. Bootstrap values of greater than 50 are shown. Species names and representative sequences as detailed in Chapters 12–14 and Appendix 1 (this volume). aGroup designated in Moncalvo (2000) as Unclassified G. applanatum B. N/A = species not included in Moncalvo (2000).

Species

All Ganoderma species form distinct brackets (fruiting bodies) from woody material where basidiospores are released from a network of pores (polyporoid). The term ‘bracket’ is commonly used to indicate that the form is ‘shelf-like’ or sessile and protruding from a substrate, although some may be produced on a stalk (stipe). Stipe formation appears to be influenced by the substrate and the environment or habitat, with species mostly adapted to growth on roots and leaf litter usually emerging on elongated stems, with those growing on dead trunk material of woody hosts being largely dimidiate or sessile. Plant-pathogenic species such as Ganoderma boninense, Ganoderma philippii and Ganoderma zonatum may express varying degrees of