Moniliophthora perniciosa

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Moniliophthora perniciosa
Crinipellis perniciosa mushroom.jpg
Scientific classification OOjs UI icon edit-ltr.svg
Domain: Eukaryota
Kingdom: Fungi
Division: Basidiomycota
Class: Agaricomycetes
Order: Agaricales
Family: Marasmiaceae
Genus: Moniliophthora
Species:
M. perniciosa
Binomial name
Moniliophthora perniciosa
(Stahel) Aime & Phillips-Mora, (2005)
Synonyms

Crinipellis perniciosa(Stahel) Singer, (1943)
Crinipellis perniciosa var. perniciosa(Stahel) Singer, (1943)
Marasmius perniciosusStahel, (1915)

Contents

Moniliophthora perniciosa (previously Crinipellis perniciosa) [1] is a fungus that causes "witches' broom disease" (WBD) of the cocoa tree T. cacao. [2] This pathogen is currently limited to South America, Panama and the Caribbean, and is perhaps one of the best-known cocoa diseases, thought to have co-evolved with cocoa in its centre of origin (first recorded in the Brazilian Amazon in 1785).

This fungus is hemibiotroph, with two characteristic phases: biotrophic (expanding and infecting, on living tissue) and saprotrophic (producing basidiospores, on necrotic tissue). The biotrophic stage, and what triggers its switch to a saprotrophic stage, are still not understood.

Hosts and symptoms

Moniliophthora perniciosa can infect a number of hosts. Generally, M. perniciosa infects tropical host plants, and host plants in the Upper Amazon River basin on the eastern side of the Andes. [3] M. perniciosa is now known to comprise four different biotypes (C, S, L and H), each infecting different (and unrelated) host plants. The economically important C-biotype infects species of Theobroma and Herrania (family Malvaceae). [4]

A second biotype (L-biotype) was found on liana vines in Ecuador; [5] subsequently the host was identified as Arrabidaea verrucosa (Bignoniaceae) but witches' broom symptoms have not been observed on this host. [6] The S-biotype, reported only from Brazil caused witches' broom symptoms on hosts within the family Solanaceae, [7] including Solanum rugosum; . Under experimental conditions, this biotype is also able to cause witches' broom symptoms on tomato, aubergine, pepper and potato. [8] Most recently discovered is the H-biotype, which infects Heteropterys acutifolia (Malpighiaceae) but this has been reclassified as a separate species, Moniliophthora brasiliensis. [9] Recent phylogenetic analysis of field-collected basidiomes and cultures suggests that other biotypes may also exist. [10]

Investigation of the breeding biology of these various biotypes found that those causing disease symptoms (C,S) are non-outcrossing (primary homothallic), wherein a single uninucleate basidiospore is capable of completing its life cycle. [11] This is crucial in the epidemiology of disease since a single spore infection can be fertile. Primary homothallism is highly unusual amongst agaric fungi which are outcrossing, requiring mating between mycelia derived from single spore germlings (monokaryons) to form a dikaryon which is capable of basidiome formation. The L-biotype, in contrast to its relatives exhibits a bifactorial outcrossing mechanism. [6]

Infection of M. perniciosa on T. cacao causes Witches’ Broom Disease (WBD), which show distinctive symptoms of hypertrophy and hyperplasia of distal tissue of the infection site, loss of apical dominance, proliferation of auxiliary shoots, and the formation of abnormal stems resulting in a broom-like structure called a green broom. [4] Infection of flower cushions results in the formation of cushion brooms and reduces the ability to produce viable pods, causing seedless pods, or in other words, parthenocarpic fruits. Parthenocarpy results in M. perniciosa targeting nutrient acquisition while altering the host physiology without causing significant necrosis. [12] After 1–2 months post infection, necrosis of infected tissues occurs distal to the original infection site, forming a structure called a dry broom. [4] WBD may also lead to plant death after successive attacks of M. perniciosa. [13] Signs of M. perniciosa infection are green brooms, which are broom-like structures that are formed from the stem, and highly infective mushrooms formed on pods and affected vegetative tissue, which are small and pink. [4] It is possible to cultivate these basidiomata under experimental conditions on a bran-vermiculite medium using the 'pie-dish' method to simulate the wetting/drying conditions experienced by the fungus under field conditions. [14]

Environment

M. perniciosa evolved from the Amazon and its susceptible hosts are tropical plants located in rain forests. [3] Favorable conditions for the disease to spread are humid, warm tropical weather. [12] The spores of this fungus are spread by wind, but must land in water in order to germinate. As a consequence, it mainly spreads during rainy periods. In most cacao production areas, rainfall totals and temperature maximums range between 1300 and 3000 mm and 30 to 33 °C. [4] These conditions are ideal for WBD development.

Disease management

Generally, there are four major strategies that can be used for disease control of Witches’ Broom. One strategy is phytosanitation, which is the removal and destruction of diseased plant parts. This can only be conducted during dry periods, or one risks spreading the disease further. Other strategies for control are chemical control, genetic resistance and biological control. Genetic resistance is currently being researched. In order to achieve durable resistance to a specific pathogen, extensive knowledge of the genetics of specific host-pathogen interaction is required. [15] Host-pathogen interaction for M. perniciosa is not fully known. Some of these strategies can be tedious and expensive, for example, 95% phytosanitation is required to achieve 50% reduction in pod loss. [4] Among the endophytic fungi associated with cacao are many species of Trichoderma . Several species of Trichoderma have been isolated from cacao and is one of the most often used biofungicides. [2] One of the isolates, T. stromaticum parasitizes the saprotrophic mycelium and basidiocarps of M. perniciosa, which reduces the formation of basidiocarps by 99% when brooms are in contact with soil and 56% in brooms remaining on trees. It can reduce pod infection by 31%. [2] This biofungicide has shown variable performance due to environmental conditions of high humidity and moisture from rainfall, which is ideal for disease development, but not necessarily ideal for optimizing biocontrol efficacy. [4]

Importance

M. perniciosa infection causes young pods to become deformed (these are called chirimoyas in Spanish), whereas infection of more mature pods will cause necrosis of seeds and render the pod worthless. This largely affects cocoa production in South American countries where their cash crop is cacao beans. In 1989, WBD was introduced to the cocoa producing state of Bahia of Brazil, where output diminished from 380,000 metric tons per year to 90,000 metric tons in the late 1990s. Due to this disease, Bahia, Brazil went from being the 3rd largest exporter of cacao beans to a net importer. [13] Lack of cacao beans could increase the price for importing countries, and also for all cocoa products. The U.S. currently imports $100 million in cacao beans annually. [2]

T. cacao L. is an understorey tropical plant, and the understorey growth of cacao helps to preserve habitat for numerous animal and bird species in these regions. With the production losses associated with WBD, tropical landowners are forced to convert their land to other production systems that usually require the destruction of the forest cover. [4] WBD does not only affect the supply of cacao, but also largely impacts the conservation of tropical environment where cacao is grown. [4]

Related Research Articles

<i>Theobroma cacao</i> Species of tree grown for its cocoa beans

Theobroma cacao is a small evergreen tree in the family Malvaceae. Its seeds, cocoa beans, are used to make chocolate liquor, cocoa solids, cocoa butter and chocolate. Native to the tropics of the Americas, the largest producer of cocoa beans in 2018 was Ivory Coast, at 2.2 million tons. Its leaves are alternate, entire, unlobed, 10–50 cm (4–20 in) long and 5–10 cm (2–4 in) broad.

<span class="mw-page-title-main">Witch's broom</span> Type of deformity in a woody plant

Witch's broom or witches' broom is a deformity in a woody plant, typically a tree, where the natural structure of the plant is changed. A dense mass of shoots grows from a single point, with the resulting structure resembling a broom or a bird's nest. It is sometimes caused by pathogens.

<i>Theobroma grandiflorum</i> Species of tree

Theobroma grandiflorum, commonly known as cupuaçu, also spelled cupuassu, cupuazú, cupu assu, or copoazu, is a tropical rainforest tree related to cacao. Native and common throughout the Amazon basin, it is naturally cultivated in the jungles of north of Brazil, with the largest production in Pará, Amazonas and Amapá, Colombia, Bolivia and Peru. The pulp of the cupuaçu fruit is consumed throughout Central and South America, especially in the northern states of Brazil, and is used to make ice creams, snack bars, and other products.

<i>Phytophthora palmivora</i> Species of single-celled organism

Phytophthora palmivora is an oomycete that causes bud-rot of palms, fruit-rot or kole-roga of coconut and areca nut. These are among the most serious diseases caused by fungi and moulds in South India. It occurs almost every year in Malnad, Mysore, North & South Kanara, Malabar and other areas. Similar diseases of palms are also known to occur in Sri Lanka, Mauritius, and Sumatra. The causative organism was first identified as P. palmivora by Edwin John Butler in 1917.

<i>Rhizoctonia solani</i> Species of fungus

Rhizoctonia solani is a species of fungus in the order Cantharellales. Basidiocarps are thin, effused, and web-like, but the fungus is more typically encountered in its anamorphic state, as hyphae and sclerotia. The name Rhizoctonia solani is currently applied to a complex of related species that await further research. In its wide sense, Rhizoctonia solani is a facultative plant pathogen with a wide host range and worldwide distribution. It causes various plant diseases such as root rot, damping off, and wire stem. It can also form mycorrhizal associations with orchids.

<i>Cephaleuros virescens</i> Species of alga

Cephaleuros virescens is an algal plant pathogen that infects tea, coffee and coconut plants, causing algal leaf spot or algal rust.

Erythricium salmonicolor is a species of fungus in the family Corticiaceae. Basidiocarps are effused, corticioid, smooth, and pinkish and grow on wood. The fungus is a commercially significant plant pathogen which has become a serious problem, especially in Brazil. Erythricium salmonicolor causes Pink Disease, most commonly in Citrus, although E. salmonicolor has a wide host range including rubber and cacao trees. Pink Disease causes branch and stem die-back due to canker formation. The cankers are recognizable by gum exudation and longitudinal splitting of the bark.

<i>Ceratobasidium cornigerum</i> Species of fungus

Ceratobasidium cornigerum is a species of fungus in the order Cantharellales. Basidiocarps are thin, spread on the substrate out like a film (effused) and web-like. An anamorphic state is frequently obtained when isolates are cultured. Ceratobasidium cornigerum is saprotrophic, but is also a facultative plant pathogen, causing a number of economically important crop diseases, and an orchid endomycorrhizal associate. The species is genetically diverse and is sometimes treated as a complex of closely related taxa. DNA research shows the species actually belongs within the genus Rhizoctonia.

Ceratocystis paradoxa or Black Rot of Pineapple is a plant pathogen that is a fungus, part of the phylum Ascomycota. It is characterized as the teleomorph or sexual reproduction stage of infection. This stage contains ascocarps, or sacs/fruiting bodies, which contain the sexually produced inoculating ascospores. These are the structures which are used primarily to survive long periods of time or overwinter to prepare for the next growing season of its host. Unfortunately, the sexual stage is not often seen in the natural field but instead the anamorph, or asexual stage is more commonly seen. This asexual stage name is Thielaviopsis paradoxa and is the common cause of Black rot or stem-end rot of its hosts.

Phytophthora megakarya is an oomycete plant pathogen that causes black pod disease in cocoa trees in west and central Africa. This pathogen can cause detrimental loss of yield in the economically important cocoa industry, worth approximately $70 billion annually. It can damage any part of the tree, causing total yield losses which can easily reach 20-25%. A mixture of chemical and cultural controls, as well as choosing resistant plant varieties, are often necessary to control this pathogen.

<i>Moniliophthora roreri</i> Species of fungus

Moniliophthora roreri is a basidiomycete fungus that causes frosty pod rot disease, one of the most serious problems for cacao production in Latin America. This disease and together with witches’ broom disease and black pod rot constitute the cacao disease trilogy. It causes serious losses in southwestern parts of South America; spores are dry and powdery and are spread easily by water movement, wind, or movement of pods; disease spread is highest during periods of high rainfall.

<i>Cacao swollen shoot virus</i> Species of virus

Cacao swollen shoot virus (CSSV) is a plant pathogenic virus of the family Caulimoviridae that primarily infects cacao trees. It decreases cacao yield within the first year of infection, and usually kills the tree within a few years. Symptoms vary by strain, but leaf discoloration, stem/root swelling, and die-back generally occur. The virus is transmitted from tree to tree by mealybug vectors. It was first discovered in Ghana in 1936, and is currently endemic in Togo, Ghana and Nigeria. Over 200 million trees have already been claimed by this disease, which has prompted Ghana to launch the most ambitious and costly eradication effort of any country in the world against a viral plant disease.

<i>Moniliophthora</i> Genus of fungi

Moniliophthora is a genus of fungi in the family Marasmiaceae. The genus was described in 1978 with M. roreri as the type species. This fungus, formerly known as Monilia roreri, causes frosty pod rot, a serious disease of Theobroma cacao.

<i>Theobroma bicolor</i> Species of tree

Theobroma bicolor, known commonly as the mocambo tree, jaguar tree, balamte, or pataxte, among various other common names, is a tree in the genus Theobroma, which also contains the better-known Theobroma cacao. It is found in Central and South America, including stretches of the Amazon rainforest in Brazil, Colombia, Ecuador, and Peru.

Black pod disease is a fungal disease of Cocoa trees. This pathogen if left untreated can destroy all yields; annually the pathogen can cause a yield loss of up to 1/3 and up to 10% of total trees can be lost completely.

Ceratocystis cacaofunesta is an ascomycete fungus that causes a wilt disease in cacao trees. It has led to significant economic losses in Latin America.

<i>Candidatus</i> Phytoplasma fraxini Species of bacterium

CandidatusPhytoplasma fraxini is a species of phytoplasma, a specialized group of bacteria which lack a cell wall and attack the phloem of plants. This phytoplasma causes the diseases ash yellows and lilac witches' broom.

Cocoa necrosis virus (CoNV) is a plant pathogenic virus of the genus nepovirus that infects Theobroma cacao en natura causing cacao necrosis disease. CoNV is considered synonymous with Strain S of cacao swollen shoot virus. Unlike Cacao swollen shoot virus, it is not transmitted by mealybugs nor vectored by aphids, beetles, or leafhoppers that also commonly infest cacao. It is serologically, distantly related to Tomato black ring virus and very distantly related to Grapevine chrome mosaic virus.

Hemibiotrophs are the spectrum of plant pathogens, including bacteria, oomycete and a group of plant pathogenic fungi that keep its host alive while establishing itself within the host tissue, taking up the nutrients with brief biotrophic-like phase. It then, in later stages of infection switches to a necrotrophic life-style, where it rampantly kills the host cells, deriving its nutrients from the dead tissues.

<i>Theobroma speciosum</i> Species of flowering plant

Theobroma speciosum is an arboriform species of flowering plant in the mallow family native to northern South America. It is the 35th most abundant species of tree in the Amazon rainforest.

References

  1. ↑ Aime, M.C.; Phillips-Mora, W. (2005). "The causal agents of witches' broom and frosty pod rot of cacao (chocolate, Theobroma cacao) form a new lineage of Marasmiaceae". Mycologia. 97 (5): 1012–1022. doi:10.3852/mycologia.97.5.1012. PMID   16596953.[ permanent dead link ]
  2. 1 2 3 4 Becker, Hank (1999). "Fighting a fungal siege on Cocao farms". Agricultural Research. 47: 4–8.
  3. 1 2 Litholder Jr., Ceso; Leal Jr., Gildemberg; Albuquerque, Paulo; Figueria, Antonio (June 14, 2015). "Differential expression of Jasmonate biosynthesis genes in cocao genotypes contrasting for resistance against Moniliophthora perniciosa". Plant Cell Rep. 34 (10): 1747–1759. doi:10.1007/s00299-015-1821-x. PMID   26071948. S2CID   16829724.
  4. 1 2 3 4 5 6 7 8 9 Meinhardt, Lyndel; Rincones, Johana; Bailey, Bryan; Aime, Catherine; Griffith, Gareth; Zhang, Dapeng; Pereira, Gancalo (2008). "Moniliophthora perniciosa, the causal agent of witches' broom disease of cacao: what's new from this old foe?". Molecular Plant Pathology. 9 (5): 577–588. doi:10.1111/j.1364-3703.2008.00496.x. PMC   6640444 . PMID   19018989.
  5. ↑ Evans, H.C. (July 1978). "Witches' broom disease of cocoa Crinipellis perniciosa) in Ecuador". Annals of Applied Biology. 89 (2): 185–192. doi:10.1111/j.1744-7348.1978.tb07689.x. ISSN   0003-4746.
  6. 1 2 GRIFFITH, G. W.; HEDGER, J. N. (June 1994). "Spatial distribution of mycelia of the liana (L-) biotype of the agaric Crinipellis perniciosa (Stahel) Singer in tropical forest". New Phytologist. 127 (2): 243–259. doi:10.1111/j.1469-8137.1994.tb04276.x. ISSN   0028-646X. PMID   33874513.
  7. ↑ BASTOS, C. N.; EVANS, H.C. (June 1985). "A new pathotype of Crinipellis perniciosa (witches' broom disease) on solanaceous hosts". Plant Pathology. 34 (2): 306–312. doi:10.1111/j.1365-3059.1985.tb01366.x. ISSN   0032-0862.
  8. ↑ Griffith, G.W.; Nicholson, J.; Nenninger, A.; Birch, R.N.; Hedger, J.N. (2003). "Witches' brooms and frosty pods: two major pathogens of cacao". New Zealand Journal of Botany. 41 (3): 423–435. doi: 10.1080/0028825X.2003.9512860 .
  9. ↑ de Arruda, M.C.C.; Sepulveda Ch., G.F.; Miller, R.N.G.; Ferreira, M.A.S.V.; Santiago, D.V.R.; Resende, M.L.V.; Dianese, J.C.; Felipe, M.S.S. (2017). "Crinipellis brasiliensis, a new species based on morphological and molecular data". Mycologia. 97 (6): 1348–1361. doi:10.1080/15572536.2006.11832741. PMID   16722225. S2CID   218588140.
  10. ↑ Artero, A. S.; Silva, J. Q.; Albuquerque, P. S. B.; Bressan, E. A.; Leal, G. A.; Sebbenn, A. M.; Griffith, G. W.; Figueira, A. (2016-11-23). "Spatial genetic structure and dispersal of the cacao pathogen Moniliophthora perniciosa in the Brazilian Amazon" (PDF). Plant Pathology. 66 (6): 912–923. doi:10.1111/ppa.12644. ISSN   0032-0862. S2CID   89033683.
  11. ↑ Griffith, G W; Hedger, J N (March 1994). "The breeding biology of biotypes of the witches' broom pathogen of cocoa, Crinipellis perniciosa". Heredity. 72 (3): 278–289. doi: 10.1038/hdy.1994.38 . ISSN   0018-067X.
  12. 1 2 Melnick, Rachel; Marelli, Jean-Philippe; Sicher, Richard; Strem, Mary; Bailey, Bryan (December 2012). "The interaction of Theobroma cacao and Moniliophthora perniciosa, the causal agent of witches' broom disease, during parthenocarpy". Tree Genetics & Genomes. 8 (6): 1261–1279. doi:10.1007/s11295-012-0513-8. S2CID   14233290.
  13. 1 2 Gramacho, Karina; Luz, Edna; Santos da Silva, Fernanda; Lopes, Uilson (2016). "Pathogenic variability of Moniliophthora perniciosa in three agroecological zones of cacao region of Bahia, Brazil". Crop Breeding and Applied Biotechnology. 16: 7–13. doi: 10.1590/1984-70332016v16n1a2 .
  14. ↑ Griffith, G. W.; Hedger, J. N. (1993-07-01). "A novel method for producing basidiocarps of the cocoa pathogen Crinipellis perniciosa using a bran-vermiculite medium". Netherlands Journal of Plant Pathology. 99 (4): 227–230. doi:10.1007/BF01974667. ISSN   0028-2944. S2CID   44201042.
  15. ↑ Silvia, D.; Araujo, I.; Branco, S.; Aguilar-Vildoso, C.; Lopes, U.; Marelli, J.; Motamayor, J.; Royaert, S.; Reboucas, R. (1997). "Analysis of resistance to witches' broom disease (Moniliophthora perniciosa) in flower cushions of Theobroma cacao in a segregating population". Plant Pathology. 63 (6): 1264–1271. doi:10.1111/ppa.12204.
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