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Phytoplasma

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Phytoplasma
Phyllody induced by phytoplasma infection on a coneflower (Echinacea purpurea).
Scientific classification
Division:
Tenericutes
Class:
Mollicutes
Order:
Acholeplasmatales
Family:
Acholeplasmataceae
Genus:
"Candidatus Phytoplasma"
Species

"Ca. Phytoplasma allocasuarinae"
"Ca. Phytoplasma americanum"
"Ca. Phytoplasma asteris"
"Ca. Phytoplasma aurantifolia"
"Ca. Phytoplasma australiense"
"Ca. Phytoplasma balanitae"
"Ca. Phytoplasma brasiliense"
"Ca. Phytoplasma caricae"
"Ca. Phytoplasma castaneae"
"Ca. Phytoplasma cirsii"
"Ca. Phytoplasma cocosnigeriae"
"Ca. Phytoplasma cocostanzaniae"
"Ca. Phytoplasma convolvuli"
"Ca. Phytoplasma costaricanum"
"Ca. Phytoplasma cynodontis"
"Ca. Phytoplasma fragariae"
"Ca. Phytoplasma fraxini"
"Ca. Phytoplasma graminis"
"Ca. Phytoplasma japonicum"
"Ca. Phytoplasma luffae"
"Ca. Phytoplasma lycopersici"
"Ca. Phytoplasma malasianum"
"Ca. Phytoplasma mali"
"Ca. Phytoplasma omanense"
"Ca. Phytoplasma oryzae"
"Ca. Phytoplasma palmae"
"Ca. Phytoplasma palmicola"
"Ca. Phytoplasma phoenicium"
"Ca. Phytoplasma pini"
"Ca. Phytoplasma pruni"
"Ca. Phytoplasma prunorum"
"Ca. Phytoplasma pyri"
"Ca. Phytoplasma rhamni"
"Ca. Phytoplasma rubi"
"Ca. Phytoplasma solani"
"Ca. Phytoplasma spartii"
"Ca. Phytoplasma sudamericanum"
"Ca. Phytoplasma tamaricis"
"Ca. Phytoplasma trifolii"
"Ca. Phytoplasma ulmi"
"Ca. Phytoplasma vitis"
"Ca. Phytoplasma ziziphi"

(as of March 2016)

Phytoplasmas are specialised bacteria that are obligate parasites of plant phloem tissue and transmitting insects (vectors). They were discovered by scientists in 1967 and were named mycoplasma-like organisms or MLOs.[1] They cannot be cultured in vitro in cell-free media. They are characterised by their lack of a cell wall, a pleiomorphic or filamentous shape, normally with a diameter less than 1 μm, and their very small genomes.

Phytoplasmas are pathogens of agriculturally important plants, including coconut, sugarcane, and sandalwood, causing a wide variety of symptoms that range from mild yellowing to death of infected plants. They are most prevalent in tropical and subtropical regions of the world. They require a vector to be transmitted from plant to plant, and this normally takes the form of sap-sucking insects such as leaf hoppers, in which they are also able to survive and replicate.

History

References to diseases now known to be caused by phytoplasmas occurred as far back as 1603 for mulberry dwarf disease in Japan.[2] Such diseases were originally thought to be caused by viruses, which, like phytoplasmas, require insect vectors, cannot be cultured, and have some symptom similarity.[3] In 1967, phytoplasmas were discovered in ultrathin sections of plant phloem tissue and named mycoplasma-like organisms (MLOs), because they physically resembled mycoplasmas[1] The organisms were renamed phytoplasmas in 1994, at the 10th Congress of The International Organization for Mycoplasmology.[3]

Morphology

Being Mollicutes, a phytoplasma lacks a cell wall and instead is bound by a triple-layered membrane.[4] The cell membranes of all phytoplasmas studied so far usually contain a single immunodominant protein (of unknown function) that makes up the majority of the protein content of the cell membrane.[5] The typical phytoplasma exhibits a pleiomorphic or filamentous shape and is less than 1 μm in diameter. As prokaryotes, phytoplasmas' DNA is found throughout the cytoplasm, rather than being concentrated in a nucleus.

Symptoms

A common symptom caused by phytoplasma infection is phyllody, the production of leaf-like structures in place of flowers. Evidence suggests the phytoplasma downregulates a gene involved in petal formation (AP3 and its orthologues) and genes involved in the maintenance of the apical meristem (Wus and CLV1).[6] Other symptoms, such as the yellowing of leaves, are thought to be caused by the phytoplasma's presence in the phloem, affecting its function and changing the transport of carbohydrates.[7]

Phytoplasma-infected plants may also suffer from virescence, the development of green flowers due to the loss of pigment in the petal cells.[8] Phytoplasma-harboring plants which are able to flower may nevertheless be sterile. A phytoplasma effector protein (SAP54) has been identified as inducing symptoms of virescence and phyllody when expressed in plants.

Many plants infected by phytoplasmas gain a bushy or "witches' broom" appearance due to changes in their normal growth patterns. Most plants show apical dominance, but phytoplasma infection can cause the proliferation of auxiliary (side) shoots and an increase in size of the internodes.[8] Such symptoms are actually useful in the commercial production of poinsettias. The infection produces more axillary shoots, which enables production of poinsettia plants that have more than one flower.[9]

Phytoplasmas may cause many other symptoms that are induced because of the stress placed on the plant by infection rather than specific pathogenicity of the phytoplasma. Photosynthesis, especially photosystem II, is inhibited in many phytoplasma-infected plants.[4] Phytoplasma-infected plants often show yellowing which is caused by the breakdown of chlorophyll, the biosynthesis of which is also inhibited.[4]

Effector (virulence) proteins

Many plant pathogens produce virulence factors (or effectors) that modulate or interfere with normal host processes in a way that is beneficial to the pathogen. [10] TCP transcription factors normally regulate plant development and control the expression of lipoxygenase (LOX) genes that are required for the biosynthesis of jasmonate. In infected Arabidopsis plants (and plants that express SAP11 transgenically), jasmonate levels are decreased. The downregulation of jasmonate production is beneficial to the phytoplasma because jasmonate is involved in plant defence against herbivorous insects such as leafhoppers, and leafhoppers have been shown to lay more eggs on AY-WB-infected plants at least in part because of SAP11. For example, the leafhopper Macrosteles quadrilineatus lays 30% more eggs on plants that express SAP11 transgenically, and 60% more eggs on plants infected with AY-WB.[10] Phytoplasmas cannot survive in the external environment and are dependent upon insects such as leafhoppers for transmission to new (healthy) plants. Thus, by interfering with jasmonate production, SAP11 'encourages' leafhoppers to lay more eggs on phytoplasma-infected plants, thereby ensuring that newly hatching leafhopper nymphs feed upon infected plants and become vectors for the bacteria.


Transmission

Movement between plants

Phytoplasmas are mainly spread by insects of the families Cicadellidea (leafhoppers), Fulgoridea (planthoppers), and Psyllidae (jumping plant lice) ,[11] which feed on the phloem tissues of infected plants, picking up the phytoplasmas and transmitting them to the next plant on which they feed. So, the host range of phytoplasmas is strongly dependent upon its insect vector. Phytoplasmas contain a major antigenic protein that makes up the majority of their cell surface proteins. This protein has been shown to interact with insect microfilament complexes and is believed to be the determining factor in insect-phytoplasma interaction.[12] Phytoplasmas may overwinter in insect vectors or perennial plants. Phytoplasmas can have varying effects on their insect hosts; examples of both reduced and increased fitness have been seen.[13]

Phytoplasmas enter the insect's body through the stylet, move through the intestine, and are then absorbed into the haemolymph.[13] From there they proceed to colonise the salivary glands, a process that can take up to three weeks.[13] Once established, phytoplasmas are found in most major organs of an infected insect host. The time between being taken up by the insect and reaching an infectious titre in the salivary glands is called the latency period.[13]

Phytoplasmas can also be spread via dodders (Cuscuta)[14] or vegetative propagation such as the grafting of a piece of infected plant onto a healthy plant.

Movement within plants

Phytoplasmas are able to move within the phloem from source to sink, and they are able to pass through sieve tube elements. But since they spread more slowly than solutes, for this and other reasons, movement by passive translocation is not supported.[15]

Detection and diagnosis

Before molecular techniques were developed, the diagnosis of phytoplasma diseases was difficult because they could not be cultured. Thus, classical diagnostic techniques, such as observation of symptoms, were used. Ultrathin sections of the phloem tissue from suspected phytoplasma-infected plants would also be examined for their presence.[1] Treating infected plants with antibiotics such as tetracycline to see if this cured the plant was another diagnostic technique employed.

Molecular diagnostic techniques for the detection of phytoplasma began to emerge in the 1980s and included ELISA-based methods. In the early 1990s, polymerase chain reaction-based methods were developed that were far more sensitive than those that used ELISA, and RFLP analysis allowed the accurate identification of different strains and species of phytoplasma.[16]

More recently, techniques have been developed that allow for assessment of the level of infection. Both quantitative PCR and bioimaging have been shown to be effective methods of quantifying the titre of phytoplasmas within the plant.[15]

Control

Phytoplasmas are normally controlled by the breeding and planting of disease resistant varieties of crops (believed to the most economically viable option) and by the control of the insect vector.[8]

Tissue culture can be used to produce clones of phytoplasma-infected plants that are healthy. The chances of gaining healthy plants in this manner can be enhanced by the use of cryotherapy, freezing the plant samples in liquid nitrogen, before using them for tissue culture.[17]

Work has also been carried out investigating the effectiveness of plantibodies targeted against phytoplasmas.[18]

Tetracyclines are bacteriostatic to phytoplasmas.[19] However, without continuous use of the antibiotic, disease symptoms reappear. Thus, tetracycline is not a viable control agent in agriculture, but it is used to protect ornamental coconut trees.[20]

Genetics

The genomes of three phytoplasmas have been sequenced: aster yellows witches broom,[21] onion yellows (Ca. Phytoplasma asteris)[22] and Ca. Phytoplasma australiense[23] Phytoplasmas have very small genomes, which also have extremely low levels of the nucleotides G and C, sometimes as little as 23%, which is thought to be the threshold for a viable genome.[24] In fact Bermuda grass white leaf phytoplasma has a genome size of just 530 kb, one of the smallest known genomes of living organisms.[25] Larger phytoplasma genomes are around 1350 kb. The small genome size associated with phytoplasmas is due to their being the product of reductive evolution from Bacillus/Clostridium ancestors. They have lost 75% or more of their original genes, so can no longer survive outside of insects or plant phloem. Some phytoplasmas contain extrachromosomal DNA such as plasmids.[26]

Despite their very small genomes, many predicted genes are present in multiple copies. Phytoplasmas lack many genes for standard metabolic functions and have no functioning homologous recombination pathways, but do have a sec transport pathway.[21] Many phytoplasmas contain two rRNA operons. Unlike the rest of the Mollicutes, the triplet code of UGA is used as a stop codon in phytoplasmas.[27]

Phytoplasma genomes contain large numbers of transposon genes and insertion sequences. They also contain a unique family of repetitive extragenic palindromes called PhREPS whose role is unknown though it is theorised that the stem loop structures the PhREPS are capable of forming may play a role in transcription termination or genome stability.[28]

Taxonomy

Phytoplasmas belong to the monophyletic order Acholeplasmatales.[8] In 1992, the Subcommittee on the Taxonomy of Mollicutes proposed the use of the name Phytoplasma in place of the use of the term MLO (mycoplasma-like organism) "for reference to the phytopathogenic mollicutes".[29] In 2004, the genus name Phytoplasma was adopted and is currently at Candidatus status[30] which is used for bacteria that cannot be cultured.[31] Its taxonomy is complicated because it can not be cultured, thus methods normally used for classification of prokaryotes are not possible.[8] Phytoplasma taxonomic groups are based on differences in the fragment sizes produced by the restriction digest of the 16S rRNA gene sequence (RFLP) or by comparison of DNA sequences from the 16s/23s spacer regions.[32] There is some disagreement over how many taxonomic groups the phytoplasmas fall into, recent work involving computer simulated restriction digests of the 16Sr gene suggest there may be up to 28 groups[33] whereas other papers argue for less groups, but more subgroups. Each group includes at least one Ca. Phytoplasma species, characterised by distinctive biological, phytopathological, and genetic properties.

  • List of Ca. Phytoplasma species, major groups and subgroups published with their common name and GenBank accession number of 16S rRNA gene sequence
  • Note: The Ca. Phytoplasma species names given in square brackets are provisional (16S rRNA sequences similarity <97.5%) and not yet published separately as new species. ‘Undetermined’ denotes Ca. Phytoplasma species’ group or subgroup status pending. 'Not assigned’ denotes Ca. Phytoplasma species status pending (16S rRNA sequences similarity >97.5%) as symptoms shown by the host plant/ insect were significantly different when infected with described strain of phytoplasma as compared to strain of same species or group.
Sr. no. Common name Phytoplasma species Group/subgroup Acc. no. Reference
1 Nigerian awka disease [Ca. P. cocosnigeriae] 16SrXXII-A Y14175 Firraro, 2004
2 Tanzanian lethal disease [Ca. P. cocostanzaniae] Undetermined X80117 Firraro, 2004
3 Loofah witches' broom [Ca. P. luffae] 16SrVIII-A AF086621 Firraro, 2004
4 Palm lethal yellowing [Ca. P. palmae] 16SrIV-A U18747 Firraro, 2004
5 Western X-disease [Ca. P. pruni] 16SrIII-A L04682 Firraro, 2004
6 Stolbur phytoplasma [Ca. P. solani] 16SrXII-A AF248959 Firraro, 2004
7 Flavescence doree [Ca. P. vitis] 16SrV-C AF176319 Firraro, 2004
8 Papaya yellow crinkle Ca. P. aurantifolia 16SrII-D Y10097 Davis et al., 1997
9 Allocasuarina yellows Ca. P. allocasuarinae Undetermined AY135523 Marcone et al., 2004
10 Potato purple top wilt Ca. P. americanum 16SrXVIII DQ174122 Lee et al., 2006
11 Lime witches' broom Ca. P. aurantifolia 16SrII-B U15442 Zriek et al., 1995
12 Grapevine yellows Ca. P. australience 16SrXII L76865 Davis et al., 1997
13 Balanites witches' broom Ca. P. balanitae 16SrV AB689678 Win et al., 2012
14 Hibiscus witches' broom Ca. P. brasiliense 16SrXV AF147708 Montano et al., 2001
15 Papaya bunchy top Ca. P. caricae 16SrXVII AY725234 Arocha et al., 2005
16 Chestnut witches' broom Ca. P. castaneae 16SrXIX AB054986 Jung et al., 2002
17 Bindweed yellows "Ca. P. convolvuli" 16SrXII JN833705 Martini et al., 2012
18 Soybean stunt Ca. P. costaricanum 16SXXXI HQ225630 Lee et al., 2011
19 Sugarcane white leaf Ca. P. cynodontis 16SrXI AB052874 Jung et al., 2003
20 Areca palm yellow leaf Ca. P. cynodontis 16SrXI-A JN967909 Ramaswamy et al., 2012
21 Sugarcane white leaf Ca. P. cynodontis 16SrXI-C X76432 Lee et al., 1998
22 Leafhopper bourne BVK Ca. P. cynodontis 16SrXIV X76429 Semuller et al., 2004
23 Bermuda grass white leaf Ca. P. cynodontis 16SrXIV AJ550985 Marcone et al., 2004
24 Cynodon white leaf Ca. P. cynodontis Undetermined AF509321 Blanche et al., 2003
25 Sorghum grassy shoot Ca. P. cynodontis Undetermined AF509324 Blanche et al., 2003
26 Sorghum grassy shoot Ca. P. cynodontis Undetermined AF509325 Blanche et al., 2003
27 Strawberry witches' broom yellows Ca. P. fragariae 16SrXII-E DQ086423 Valiunas et al., 2006
28 Ash yellows Ca. P. fraxini 16SrVII-A AF092209 Griffiths et al., 1999
29 Sugarcane Yellow Leaf "Ca. P. graminis" 16SrXVI AY725228 Arocha et al., 2005
30 Hydrangea phyllody Ca. P. japonicum 16SrXII-D AB010425 Sawayanagi et al., 1999
31 Parsley leaf of tomato Ca. P. lycopersici" Undetermined EF199549 Arocha et al., 2007
32 Periwinkle phyllody Ca. P. malasianum 16SrXXXII EU371934 Nejat et al., 2012
33 Apple proliferation Ca. P. mali 16SrX-A AJ542541 Semuller et al., 2004
34 Cassia italica witches' broom Ca. P. omanense 16SrXXIX EF666051 Saddy et al., 2008
35 Rice yellow dwarf Ca. P. oryzae 16SrXI-A D12581 Namba et al., 2009
36 Rice yellow dwarf Ca. P. oryzae 16SrXI-A AB052873 Jung et al., 2003
37 Almond lethal disease Ca. P. phoenicium 16SrIX-D AF515636 Verdin et al., 2003
38 Pine shoot proliferation Ca. P. pini 16SrXXI AJ632155 Schneider et al., 2005
39 Prunus X-disease Ca. P. pruni 16SrIII-A JQ044393 Davis et al., 2012
40 European stone fruit Ca. P. prunorum 16SrX-F AJ542544 Semuller et al., 2004
41 Pear decline Ca. P. pyri 16SrX-C AJ542543 Semuller et al., 2004
42 Buckthorn witches' broom Ca. P. rhamni 16SrXX X76431 Marcone et al., 2004
43 Rubus stunt Ca. P. rubi 16SrV AY197648 Maher et al., 2011
44 Bois nor Ca. P. solani 16SrXII JQ730746 Quaglino et al., 2013
45 Spartium witches' broom Ca. P. spartii 16SrX-D X92869 Marcone et al., 2004
46 Passiflora witches' broom Ca. P. sudamericanum 16SrIII-V GU292082 Davis et al., 2012
47 Passiflora witches' broom Ca. P. sudamericanum 16SrVI GU292081 Davis et al., 2012
48 Salt cedar witches' broom Ca. P. tamaricis 16SrXXX FJ432664 Zhao et al., 2009
49 Clover proliferation Ca. P. trifolii 16SrVI-A AY390261 Hiruki et al., 2004
50 Elm yellows Ca. P. ulmi 16SrV-A AY197655 Lee et al., 2004
51 Jujube witches' broom Ca. P. ziziphi 16SrV-B AB052876 Jung et al., 2003
52 Aster yellows Ca. P. asteris 16SrI M30790 Lee et al., 2004
53 MexiCan periwinkle virescence Not assigned 16SrXIII-A AF248960 Wei et al. 2007
54 Bermuda grass white leaf Not assigned 16SrXIV AJ550984 Marcone et al., 2004
55 Grapevine yellow Not assigned 16SrXXIII-A AY083605 Wei et al., 2007
56 Sorghum bunchy shoot Not assigned 16SrXXIV-A AF509322 Wei et al., 2007
57 Weeping tea witches' broom Not assigned 16SrXXV-A AF521672 Wei et al., 2007
58 Sugarcane yellows Not assigned 16SrXXVI-A AJ539179 Wei et al., 2007
59 Sugarcane yellows Not assigned 16SrXXVII-A AJ539180 Wei et al., 2007
60 Derbid phytoplasma Not assigned 16SrXXVIII-A AY744945 Wei et al., 2007
61 Chinaberry yellows Not assigned Undetermined AF495882 Wei et al., 2007

See also

References

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  33. ^ Wei, W; Davis, RE; Lee, IM; Zhao, Y (2007). "Computer-simulated RFLP analysis of 16S rRNA genes: identification of ten new phytoplasma groups". International Journal of Systematic and Evolutionary Microbiology. 57 (Pt 8): 1855–1867. doi:10.1099/ijs.0.65000-0. PMID 17684271. {{cite journal}}: Unknown parameter |name-list-format= ignored (|name-list-style= suggested) (help)
  34. ^ Yadav, A.; Bhale, U.; Thorat, V.; Shouche, Y. (2014). "First Report of new subgroup 16SrII- M 'Candidatus Phytoplasma aurantifolia' associated with 'Witches Broom' disease of Tephrosia purpurea in India". Plant Disease. 98: 990. doi:10.1094/PDIS-11-13-1183-PDN.
  35. ^ Nasare, K.; Yadav, Amit; Singh, A. K.; Shivasharanappa, K. B.; Nerkar, Y. S.; Reddy, V. S. (2007). "Molecular and symptom analysis reveal the presence of new phytoplasmas associated with sugarcane grassy shoot disease in India". Plant Disease. 91 (11): 1413–1418. doi:10.1094/PDIS-91-11-1413.
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