Introduction
Palms
belong to the Arecaceae family, which comprises about 180 genera and
2600 species. They are ecologically and economically important as they provide
humans with medicine, food, and fuel and are commonly used for ornamental
purposes (Chao and Krueger 2007). Amongst
these species, three are most important, including date palm (Phoenix dactylifera
L.), coconut (Cocos nucifera L.), and the African oil palm (Elaeis
guineensis L.). Date palm is the most important fruit crop in the Middle
East, North Africa, and Arabian Peninsula. This crop was also introduced in
India, southern Africa, South America, Australia, and the United States. Based
on FAO statistics, date palm production significantly increased from 1.8
Million ton (Mt) in 1962 to 8.5 Mt in 2018, which Egypt been the first in date
production (1.6 Mt), followed by Saudi Arabia (1.3 Mt), Iran (1.2 Mt) and
Algeria (1.1 Mt) (FAO 2019). Coconut
palm, with a total cultivated area of 12 million ha and 62 million tone of
production, is grown in tropical areas (mainly in Asia) in 90 countries and it
is the main income source and staple food for many developing countries (FAO 2019). Oil palm production reached 272
Million tons in 2018 from about 19 million ha of cultivated area (FAO 2019).
Phytoplasmas are wall-less prokaryotes associated with
more than 600 diseases (Maejima et al. 2014; Kumari et al. 2019; Solomon et al.
2019). They are transmitted by phloem-sucking insects in the families
Cicadellidae, Cixiidae, Cercopidae, Derbidae, Delphacidae and Psyllidae (Weintraub and Beanland 2006; Linck and Reineke 2019;
Quaglino et al. 2019;
Jakovljević et al. 2020)
and colonize the vector by entering the midgut lumen, adhering to midgut
epithelium cells eventually invading the hemolymph and reaching the salivary
glands for further dissemination (Marzachì 2004).
There are several reports on the transovarial transmission of phytoplasmas to
the progeny by infected females (Kawakita et al. 2000; Tedeschi et al. 2006; Mittelberger et al. 2017).
In this review, up-to-date information is provided about
phytoplasma associated with palm diseases, vectors, management methods and
phytoplasma biology and interaction with palms.
Lethal
Yellowing Diseases
Lethal
yellowing diseases (LYD) are defined as a syndrome with similar and specific
symptoms (Gurr et al. 2016; Solomon et al.
2019). Lethal yellowing is also called lethal decline, lethal yellowing
type syndrome, and coconut lethal yellowing (Narvaez et al. 2016; Bahder et al. 2017). It is caused by many groups and subgroups of
phytoplasma in the world. The incidence and appearance of the symptoms vary
greatly depending on host species, variety, phytoplasma group, and geographical
location (Harrison et al. 2014). General symptoms observed in all LYD are the
drop of the immature and ripe fruits (Mazivele et al. 2018). The tips of the
fronds become yellow in color, especially on the oldest fronds, followed by
falling of fronds from the stem (Bila et al. 2019; Pilet et al. 2019; Solomon et al.
2019).
LYD was first observed and reported from the Caribbean
in the 1800s, followed by Ghana, Tanzania, and Togo (Dollet et al. 2009). An
outbreak of “coconut bud rot” resulted in extensive yield loss and stopped the
commercial production in the Caribbean (Johnson
1912). Simultaneously, an epidemic was reported from Jamaica, Honduras,
southern Mexico, Florida, Cuba, Haiti, Bahamas, and Belize (Harrison et al.
2002a; Baudouin et al. 2008; Lebrun et al. 2008; CABI 2012). Because
of the similarity of the typical symptoms in hosts in different parts of the
world, researchers suspected that they had the same causative agent. However,
the differences in symptom progression raised a question that there may be
different pathogens. The development in the identification techniques,
especially molecular identification, helped characterize the different groups
and subgroups of phytoplasma associated with this syndrome (Table 1) (Dollet et al.
2009; Eziashi and Omamor 2010; Bertaccini
et al. 2014; Contaldo et al.
2019; Córdova et al. 2019; Zamharir and
Eslahi 2019).
Currently, this disease is considered an important issue
in the coconut production industry in Central America and the Caribbean (Ntushelo et al.
2013). This disease is presently occurring in Nigeria, Mozambique,
Ghana, Benin, Lenya, Togo, Tanzania, India, Sri Lanka, Indonesia (Table 1) (Dollet et al.
2009; Eziashi and Omamor 2010; Perera et
al. 2012; Ramjegathesh et al.
2012, 2019). Smallholder and subsistence farmers were more affected by
the lethal yellowing disease due to their heavy reliance on coconut nutrition
and economy (Myrie et al. 2011).
LYD is widely reported from coconut (Fig. 1), although
it also occurs on date palm and oil palm (Kra et al. 2017; Zamharir and Eslahi 2019).
Table 1 presents the other palm species host of LYD. The most devastating
outbreak has been reported on coconut. For example, 86% of coconut trees died
from 1961 to 1983 in Jamaica (Jones 2002).
Other outbreaks referred to as “Akwa wilt”, “Cape St. Paul Wilt”, and
“Kian-cope” diseases killed millions of coconuts in Nigeria, Ghana, and Togo,
respectively (Eziashi and Omamor 2010).
It is estimated that 38% of coconut trees were destroyed in Tanzania since the
1960s (Mugini 2002). This disease is not
always “lethal”, and slight symptoms were observed in other species like date
palm (Manimekalai et al. 2014a; Zamharir and Eslahi 2019).
The first report of an association between phytoplasma
and date palm dates back to 1998 when Tymon et al. (1998) reported the
association of 16SrIV-C with silver date palms. Two years later, slow decline,
or El Arkish was reported from Sudan in which 16SrXIV was found associated with
this disease (Cronjé et al. 2000). In 2002, date palm yellows associated
with 16SrIV-A was reported from Kuwait (Al-Awadhi et al. 2002), which was the first
report of phytoplasma disease occurring in date palms in Asia. Al-Wijam
disease, associated with 16SrI-B phytoplasma, was observed in Saudi Arabia in
2007 (Alhudaib et al. 2007). In addition, the 16SrII phytoplasma has been
found associated with date palm in Saudi Arabia (Omar et al. 2018). In America,
16SrIV-F was first reported on date palm in 2013 (Ntushelo et al. 2013). Alkhazindar (2014) reported the association of
16SrI phytoplasma with date palm in Egypt. Recently, the 16SrVI-A and VII-A
phytoplasmas were reported on date palms in Iran (Zamharir et al. 2016; Zamharir
and Eslahi 2019). Although phytoplasma diseases on date palm are not
lethal so far, significant economic losses were observed in this region (Fig.
2). For example, fruit failure at harvest has been reported due to Al-Wijam in
Kuwait and Saudi Arabia (Alhudaib et al. 2007).
Origin and
causes of LYD
According to the report of LYD outbreak in the Caribbean, it is
speculated that the disease originated in this region (Johnson 1912). However, this hypothesis was rejected by Ogle and Harries (2005), who stated that
coconut palms were healthy after introduction to this region for several
hundred years in the 16th century. Importing grasses from India to
the Caribbean is the recent hypothesis indicating that insects harboring
phytoplasma could have transferred to the Caribbean on cattle fodder in the 19th
century. This speculation is supported by the fact that West Africa was the
destination of fodder transportation from India, where LYD occurred (Ogle and Harries 2005). Taking into account
the above facts, it can be hypothesized that the origin of LYD was in Asia (Ogle and Harries 2005). However, by the
identification and discovery of many associated phytoplasma groups with LYD, it
has been suggested that there were diverse origins. For instance, according to
the low mortality of Sabal Mexicana (Texas palmetto), Vázquez-Euán et
al. (2011) suggested the phytoplasma 16SrIV-D could have originated
in Mexico. Lethal yellowing disease occurred when a vector was introduced in
new areas indicating the non-native origin of the disease in the Caribbean (Elliott 2009), while the potential vectors of
the recent epidemic of Bogia coconut syndrome are all native species in Papua
New Guinea (Pilotti et al. 2014). Additional information regarding the
discovery and naming can be found in Lee et al. (2007).
Phytoplasmas are classified into groups and subgroups by
comprising the gene targeting the 16S ribosomal gene sequences. Currently, 44
groups and more than 100 subgroups have been identified and are yearly
increasing. In addition to this gene, other genes like tuf, secA, rp, groEL,
secY, and the 16S-23S rRNA spacer region are used for further distinction (Seruga Musić
et al. 2014; Al-Subhi et al.
2018; Balakishiyeva et al. 2018;
El-Sisi et al. 2018; Jamshidi et al. 2019; Oliveira et al. 2020). Also, specific
antibodies, vector transmission, and host range can be used for additional
discrimination (Fránová et al. 2013; Ntushelo et al.
2013).
%20631-644%20Rev_files/image002.jpg)
Fig. 1: A map indicating distribution of
phytoplasma diseases in most important species of palms
%20631-644%20Rev_files/image004.png)
Fig. 2: Symptoms of
yellowing and leaf stunting in Phoenix dactylifera associated with
16SrII-D phytoplasma
LYD Phytoplasmas are commonly classified into the 16SrIV
group, although some have now been reclassified into the groups 16SrXXII (Harrison et al.
2014), 16SrI, 16SrXI, and 16SrXIV (Bertaccini et al. 2014) (Fig. 3). Based on
vectors, plant hosts, and variety, the 16SrIV group is divided into six
subgroups A–F (Martinez et al. 2008; Vázquez-Euán et
al. 2011). These subgroups might vary in symptoms, host range, and
vectors. For instance, 16SrIV-A affect palms 18 months and older; another
subgroup of 16SrIV (not given) could infect bearing and non-bearing palms (Harrison et al.
2002b). Different phytoplasma groups have been reported in different
regions. For example, it has been demonstrated that the prevalent groups in
West and East Africa are XXII-B, IV-C, and a new unclassified
coconut-associated phytoplasma (Bila et al. 2015). On the other hand,
16SrXIV and 16SrXXIII groups have been reported from Malaysia (Nejat et al.
2009b).
%20631-644%20Rev_files/image006.jpg)
Fig. 3: A phylogenetic
tree representing phytoplasma groups and subgroups associated with palms
Numerous plant species and/or varieties of palm are
infected with some phytoplasma subgroups (Table 1). In Mexico, 16SrIV-A is
found in T. radiate and C. nucifera in the same area, while Pseudophoenix
sargentii and S. mexicana are affected by 16SrIV-A. Also,
it is likely that one subgroup only infects a palm species (Table 1). However,
mixed infection with subgroups of a group in one palm species is not unexpected
as S. mexicanat could be a host of 16SrIV-D and 16SrIV-A (Fránová et al.
2013).
Spread of phytoplasma-associated palm diseases
LYD phytoplasmas
can be spread via different means. Oropeza et al. (2017) confirmed that
seed transmission could occur in LYD from embryos to plantlets by in vitro
germination of the zygotic embryo of infected seeds. Phytoplasmas can also
spread via movement of infected plant materials (Cordova et al. 2003). Geographical
barriers such as mountain ranges can significantly affect the rate of spread (CABI 2012). Human activity could play a
substantial role in the spread of plant diseases globally, including LYD. In
Mexico, for example, studies found that the export of palms and grasses from
Florida introduced LYD to Mexico before spreading to Central America. Other
diseases have been introduced to a new area in as the same scenario (Bertin et al.
2007).
Vectors
play a crucial role in phytoplasma distribution and spread (Rashidi et al.
2014; Linck and Reineke 2019). Although many papers have been published
on phytoplasma vectors, the vectors of many phytoplasmas Table 1: Current distribution, phytoplasma groups and host plants
of phytoplasma diseases on palms
|
Location |
Name |
16Sr Group |
Host |
References |
|
Asia |
||||
|
Iran |
Streak yellow date palm |
VI-A, VII-A |
Phoenix dactylifera |
(Zamharir and Eslahi 2019) |
|
Kuwait |
Yellows date palm |
IV-A |
P. dactylifera |
(Al-Awadhi et al. 2002) |
|
King Saudi Arabia |
Al-wijam |
I-B |
P. dactylifera |
(Alhudaib et al. 2007) |
|
lethal Yellowing palm disease |
II-D |
P. dactylifera |
(Omar et al. 2018) |
|
|
Lethal yellowing Mexican fan palm |
Washingtonia
robusta |
|||
|
India |
Kerala wilt disease |
IV-C |
Coconut
nucifera |
(Edwin and Mohankumar 2007) |
|
India |
Root (wilt) disease |
XI-A, XI-B |
C.
nucifera |
(Manimekalai et al. 2014b;
Yadav et al. 2015) |
|
India |
Oil palm stunting (OPS) |
I-B |
Elaeis
guineensis |
(Mehdi et al. 2012) |
|
Sri Lanka |
Weligama coconut leaf wilt disease |
XI |
C.
nucifera |
(Perera et al. 2012; Kumara et al. 2015) |
|
Malaysia |
Coconut yellow decline |
XIV |
C.
nucifera |
(Nejat et al. 2009a, c) |
|
Malaysia |
Ca. P. malayasianum |
XXXII-B, XXXII-C |
C.
nucifera, E. guineensis |
(Nejat et al. 2013) |
|
Malaysia |
Coconut lethal yellowing (CLY) |
XIV-A, I-B, XXXVI-A |
Wodyetia
bifurcata |
(Naderali et al. 2013, 2017) |
|
Malaysia |
Royal pam yellow decline |
I |
Roystonea
regia |
(Naderali et al. 2015) |
|
Malaysia |
Coconut yellow decline |
I-B |
Cyrtostachys renda |
(Naderali et al. 2014) |
|
Indonesia |
Kalimantan wilt and natura wilt |
XI, XIII |
C. nucifera |
(Ogle and Harries 2005; Warokka et
al. 2006) |
|
Africa |
||||
|
Nigeria |
Awka disease |
XXII-A |
C.
nucifera |
(Ekpo and Ojomo 1990; Tymon et al.
1998; Wei et al. 2007; Osagie et al. 2015) |
|
Tanzania |
Coconut lethal disease |
IV-C |
P.
dactylifera |
(Tymon et al. 1998) |
|
Kenya |
Coconut lethal disease |
IV-C |
C.
nucifera |
(Córdova et al. 2014) |
|
Mozambique |
Coconut lethal disease |
IV-B, IV-C,
XXII-A |
C.
nucifera |
(Córdova et al. 2014; Harrison et al. 2014; Bila et al. 2015) |
|
Ghana, Cote d’Ivoire, Nigeria, Togo, Cameron, Benin |
Cape St. Paul wilt, CSPW keta disease, Kinacope, Kribi
disease or Cote d’Ivoire lethal yellowing disease |
XXII-B, XXII-C |
C.
nucifera, Elaeis guineensis, Borasus aethiopium, Raphium vinifera |
(Harrison et al. 2014;
Arocha-Rosete et al. 2015; Osagie et al. 2015; Kra et al. 2017) |
|
Egypt |
Date palm yellows |
I-B |
P.
dactylifera |
(Alkhazindar 2014) |
|
Sudan |
Slow decline or El Arkish, or White Tip die-back |
XIV |
P.
dactylifera |
(Cronjé et al. 2000) |
|
America |
||||
|
Florida |
Coconut lethal yellowing (CLY) |
IV-F |
W.
robusta, P. dactylifera |
(Harrison et al. 2008;
Ntushelo et al. 2013) |
|
Dominican
Republic |
CLY |
IV-E |
C.
nucifera |
(Martinez et al. 2008;
Ntushelo et al. 2013; Córdova et al. 2014) |
|
Mexico, Honduras |
Yucatan coconut lethal decline, lethal yellowing
disease |
IV-B |
C.
nucifera, Acrocomia auleata |
(Roca et al. 2006; Ntushelo et al. 2013) |
|
Florida, Caribbean Basin |
CLY |
IV-A |
C.
nucifera and 38 other palm species |
(Gurr et al. 2016) |
|
Mexico, Texas
and Florida, Puerto Rico |
Texas Phoenix palm decline (TPPD) C. palmate
yellows (CPY) phytoplasma or Sabal Mexicana lethal decline, Lethal yellowing-like syndrom |
IV-D IV-A |
P.
canariensis, P. dactylifera, P. reclinata, P. roebelenii, P. sylvestria,
Sabal palmetto, Syagrus romanzoffiana, Carlodovica palmate, Sabal Mexicana,
Pseudophoenix sargentii, Pritchardia pacifica, Thrinzaradiata, Carpentaria
acuminate, Caryota mitis, Roystonea spp., Adonidia merrillee; Tharinax radiate, Coccothrinax readii; Roystonea regia; Acrocomia mexicana |
(Harrison et al. 2002c;
Narvaez et al. 2006; Vázquez-Euán et al. 2011; Córdova et al. 2014; Narvaez et al. 2016; Lara et al. 2017) |
|
Colombia |
Oil palm lethal wilt |
I-B |
Elaeis
guineensis |
(Alvarez et al. 2014) |
|
Florida (Hossonborg county) |
Lethal bronzing disease of palm |
IV-D |
Syagrus
romanzoffiana, Sabal palmetto |
(Bahder et al. 2018) |
|
Florida |
Texas phoenix palm decline (TPPD) |
IV-D |
Bismarckia
nubilis |
(Dey et al. 2018) |
|
Louisiana |
Lethal yellowing |
IV-A, IV_D |
P.
sylvestris; Trachycarpus fortunei |
(Singh and Ferguson 2017; Ferguson and Singh 2018) |
|
Cuba |
Lethal yellowing |
IV-A |
C.
nucifera |
(Llauger et al. 2002) |
|
Guatemala |
Lethal yellowing |
IV-A |
C.
nucifera |
(Mejía et al. 2004) |
|
Jamaica |
Lethal yellowing |
IV-A |
C.
nucifera |
(Myrie et al. 2007) |
|
Oceania |
||||
|
Papua new Guinea, Solomon Islands |
Banana wilt associated phytoplasma (BWAP) |
XXII-A |
C.
nucifera |
(Davis et al. 2015) |
still to be identified. Auchenorrhyncha and
Sternorrhyncha comprise most vectors of phytoplasmas (Howard et al. 2001).
Palms are hosts for many Auchenorrhyncha, although most of them do not cause a
direct injury. Having the ability to vector pathogens makes them the most
important threat to palms. Insects should be able to acquire and retransmit
phytoplasma to the healthy plants in order to be considered a vector (Bosco and Tedeschi 2013). The only confirmed
LYD vectors are Haplaxius crudus (van Duzee) in Florida (Howard et al.
1983) and Proutista moesta in India (Rajan 2013). Putative vectors of LYD
phytoplasmas are listed in Table 2.
Alternate
Hosts of LYD
Different
palm species and few non-palm related species are considered as alternative host
plants of LYD in Florida (Gurr et al. 2016; Rosete et al. 2016). Mixed infection of 16rXXII-A with a new group
of LYD was Table 2: A list of the
vectors of lethal yellowing disease
|
Location |
Disease
name/ Phytoplasma group |
Vector |
Testing
technique |
status |
references |
|
Florida |
Lethal
yellowing/16SrIV-A |
Haplaxius
crudus |
Cage
transmission test |
confirmed |
(Harrison et al.
2008) |
|
Mexico |
Lethal
yellowing/16SrIV-A, IV-D, IV-E |
H.
crudus |
Observation/PCR |
Suggested/Putative
|
(Córdova et al.
2014; Narváez et al. 2018) |
|
Ghana |
Cape
St. Paul Wilt/16SrXXII |
Myndus
apiopodoumensis |
Cage
trials were unsuccessful but detected positive in PCR |
Putative |
(Pilet et al.
2009) |
|
Mozambique |
Coconut
lethal yellow syndrome/ 16SrXXII |
Platacantha
lutea, Diostrombus mkurangai |
PCR |
Putative |
(Dollet et al.
2011; Bila et al. 2017) |
|
Tanzania |
Coconut
lethal disease/16SrIV-C |
Diastrombus
mkurangai |
PCR |
Putative |
(Mpunami et al.
2000) |
|
India |
Kerala
wilt disease |
Stephanitis
typical, Proutista
moesta, |
Cage
transmission |
Positive |
(Mathen et al.
1990) |
|
Sophonia
greeni |
Survey/
PCR |
Putative/negative |
(Rajan 2013) |
||
|
Sri
Lanka |
Weligama
coconut leaf wilt disease/16SrXI |
Zophiuma
pupillata |
PCR |
Putative |
(Pilotti et al.
2014) |
|
Cote
D’Ivoire |
Cote
D’Ivoire lethal yellowing/ 16SrXXII-B |
Nedutepa curta |
PCR |
Putative |
(Kwadjo et al.
2018) |
detected in
coconut farms near pine trees. The new group (closely related to Ca. P.
pini, 16SrXXI) is suggested to infect coconut palms as well as the pine (Bila et al.
2015). Attempts to find alternative host plants in Jamaica revealed that
some weeds being the host of 16SrIV-A, including Synderella nodiflora
and Emilia fosbergii. The number of alternative host plants
increased, in which Cleome rutidosperma, Stachytrapheta jamaicensis
and Macroptilium lathyroides were known to be infected by
16SrIV-E (Brown and McLaughlin 2011). Danyo (2011) reported Desmodium adscendeus
were positive in PCR when screening for alternative hosts for Cap St. Paul Wilt
disease.
In addition to the alternative hosts of phytoplasmas,
plants including acid limes grown under certain environmental conditions, are
subject to phytoplasma infection without developing disease symptoms (Marcone 2014; Al-Ghaithi et al. 2017). Detection phytoplasma in such plants by PCR
cannot specify if phytoplasma presence is for a short time feeding of the
visiting insects or if the plant is an actual alternative host of the
phytoplasma (Bertaccini et al. 2014). These plants may be considered more important
than the alternative hosts developing symptoms, as they may act as a source of
phytoplasma without been noticed.
Phytoplasma
Interaction with Vectors and Host Plants
Pacifico et al. (2015) suggested that phytoplasmas change their metabolism to
adapt to new hosts. Phytoplasma infection can alter the expression and
signaling level of host plant genes, which can affect plant development (Himeno et al.
2011; Bel and Musetti 2019; Wei et al.
2019; Parakkunnel et al. 2020).
Makarova
et al. (2015) studied the genomic response of the host plants and
vectors. They revealed that 34 genes in the vector and 74 genes in the host
plants were up regulated after infection, indicating the role of genes in host
adaptation. Nejat et al. (2015) revealed that coconut, ecotype Malayan Red
Dwarf, has downregulated more genes (21860 unigene) than the upregulated ones
(18013 unigene) in response to 16SIV-related strain infection. Most genes were
responsible for innate immunity, chlorosis, and biosynthesis of secondary
metabolites. The changes of endogenous cytokinin content in response to LYD
phytoplasma revealed that cytokinin levels drastically decreased in the
infected plants compared to the healthy ones (Aguilar et al. 2009). They stated that
the symptom appearance in the host plants is due to the changes in cytokinin
level.
Phytoplasmas live in the phloem and can be found in the
sieve elements of infected plants (Santi 2019;
Zimmermann et al. 2019). It
has been demonstrated that the disruption of the carbohydrate transport system
and the photosystem II reaction center efficiency by phytoplasmas result in LYD
symptoms (Maust et al. 2003). Coconut infected by RWB increased hydrogen
peroxide and super oxide anion (Sunukumar et al. 2014).
The relationship between the plant host and the vector
can play a crucial role in the disease management (Gonella et al. 2019; Tedeschi
and Bertaccini 2019; Weintraub et al.
2019). In epidemiology, the chance of outbreak will increase if there
are two factors, the completion of one generation of the vector, and
reacquiring phytoplasma from that plant host (Oppedisano et al. 2020). Some phytoplasma
can complete their generation on one non-crop species, and therefore, the plant
may die and acquiring phytoplasma by the vector will not occur. Bios Noir
(lethal disease of grapevines in Europe) is one example of this issue. Insect
vectors feeding on palms do not complete their life cycle. In addition, it has
been demonstrated that mature palms are susceptible to LYD. Some vector species
feed on only mature palm species and infrequently found on immature ones (Howard et al.
2001). On the other hand, BCS in PNG is susceptible at all growth stages
to LYD (Kelly
et al. 2011).
Transovarial transmission of phytoplasma in the vectors
has been recently reported (Alma et al. 2019; Tedeschi and Bertaccini
2019). Vectors harboring phytoplasma were reared, and offspring were
hatched and reared on healthy plants. The new nymphs were positive in PCR and
were able to transmit the phytoplasma to the new host plants (Hanboonsong et
al. 2002; Weintraub and Beanland 2006).
Mixed infection has been observed in polyphagous insect
vectors with closely related phytoplasmas (Brown et al. 2006; Rashidi et al. 2014). For example, Euscelidius
variegatus can acquire CYP (chrysanthemum yellows phytoplasma) and FDP
(Flavescence doreé phytoplasma). It has been reported that FDP can be affected
by CYP, and CYP was dominant in its body regardless of the order of infection.
Due to the facts that CYP had a shorter latent period and FDP cannot multiply
in the salivary gland, CYP is dominant than FDP in the vector body (Rashidi et al.
2014).
Some phytoplasmas have a positive relationship with their
vectors, which can be designated as mutualistic (Queiroz et al. 2016; Galetto et al. 2018). For example, AYPs
(Aster yellows phytoplasma) increased their host range preference as well as
the fecundity of the vector. Such a relationship shows that there is a
long-time association between them (Beanland et al. 2000; Ebbert and Nault 2001).
Conversely, some phytoplasmas decreased the fitness of the vector such as the
decrease in longevity, body size and fecundity (Malagnini et al. 2010; Mayer et al. 2011).
Infected host plants are more preferred by the vectors
as indicated in some pathosystems (MacLean et al. 2014; Krüger et al. 2015). Nevertheless, phytoplasma infected Cacopsylla
picta, the vector of “Ca. P. mali”, do not prefer to oviposit on
infected than un-infected trees (Mayer et al. 2011).
Management
Presently
there is no curative treatment for LYD, though some success in controlling the
outbreaks has been reported. An integrated pest and disease management
suggested by Black, a pioneer of palm growers, has been the most successful
approach in reducing the incidence of LYD (Gurr et al. 2016). This approach
focuses on on-farm quarantine, severe weekly surveillance, and cutting down and
burning of symptomatic palms. It is also recommended to plant resistant and
high yielding varieties, controlling weeds in the whole farm and using a good
fertilization schedule (Myrie et al. 2012). A significant
reduction in the number of LYD infected palms was observed in four farms using
Black’s method, while three farms continued to be destroyed by the disease
without any management. The farms with daily surveillance lost only 0.0001% (10
out of 62000) of palms, while other farms lost thousands of palms annually (Serju 2012).
To slow the spread of LYD, the eradication of the
infected palms is highly recommended in other parts of the world. This method
was used in the Dominican Republic, as they implemented an eradication program
combined with natural barriers stopping vector movement and profusion of
resistant palms (Martinez et al. 2008, 2010). Along with ground inspection in Ghana,
aerial surveillance was employed to detect infected palms showing green against
the yellow canopy of infected palms. Recently, the drone (crewless aerial
vehicles) equipped with cameras has come to help humans in large-scale surveys.
The instant eradication of infected trees and cultivation of a resistant
variety has slowed the spread of the disease (Nkansah-Poku et al. 2009). In addition, it
has been reported that farmers burn the felled trees in Jamaica (Serju 2012). This method has not effectively
slowed the spread, because the felled palms are not attractive to the vectors.
A research conducted by Nkansah-Poku et al. (2005) in Ghana revealed
that using insecticides followed by felling had no significant effect than
felling alone in stopping the spread.
Quarantine
LYD can
spread amongst close palm farms and also to hundreds of kilometers. Vector
movement can be prohibited by natural landscape barriers. However, human
activity can spread the disease even in the presence of barriers (Bertin et al.
2007). In Mexico, grasses are imported for landscaping, and the vectors
may come through this importation (Dollet et al. 2009), unless quarantine
measures are applied strictly.
Vector
management
Alternate
vector hosts
For the
univoltine vector, the control of alternative hosts of a vector can be the most
crucial approach of controlling phytoplasma diseases (Belien et al. 2013). For
instance, Haplaxius crudus nymphs, a known vector of LYD, feed and
develop on herbaceous plants root, while the adults live on trees and palms (Howard 1995). Four species of Cyperaceae and
37 species of Poaceae were identified to be the host of H. crudus
nymphs. Grasses which are not potential host and shade-tolerant can be selected
to be replaced with alternative hosts. Howard
(1995) introduced some species that can be planted under palms as
non-hosts, including Hemarthria altissima (Pior), Brachiaria
brizantha (A. Rich) and Chloris gayana Kunth.
Mulches could be considered as a control approach. For
instance, mulches of subtle pine, coconut frond, and eucalyptus are more
attractive for female oviposition. Also, they provide better conditions for
developing nymphs, resulting in higher adult emergence. On the other hand,
using bark nuggets can result in less adult emergence (Howard and Oropeza 1998). It can be noted that mulch application
is too expensive and practical.
Insecticides
Palms are evergreen
and long living, so the vectors are able to transmit phytoplasmas anytime,
contrary to temperate, and annul crops needing protection only for short times
of susceptibility (Gitau et al. 2009). Palms are the host of many insect species, so
the use of broad-spectrum insecticides can destroy the food chain of
parasitoids and predators. In addition, the wider environment and human health
are threatened by persistent pesticides (Stehle
and Schulz 2015; Gangireddygari et al.
2017). Trunk injection and spraying insecticides are used for
controlling the vector, although it has not been economically successful in
coconut farms (Been 1995). Similarly, the
control of Kerala Wilt Disease (KWD) in India was not successful using
insecticides (Rajan 2013). In addition, a similar result was reported in
Florida where the population of the vector and spread of the disease was
reduced, but without stopping infection (Been
1995).
Host plant
resistance
Jarausch et al. (2013) defined resistant and tolerant cultivars as the absence
of symptoms associated with a low pathogen titer in the infected plants and
mild symptoms under a light pathogen titer, respectively. It should be noted
that complete resistance to LYD phytoplasma has not been reported (Baudouin et al.
2009).
As palms have to pass more time to be reproducible as
well as produce few seeds per plant, genetic modifications and improvements are
so difficult (Cardeña et al. 2003). Also, because the latent period in palms is
long, resistance screening of current genotypes is also difficult. However,
detection of phytoplasma can be more accessible, reliable, and faster by PCR
technology (Valiunas et al. 2019; Gholami et al.
2020; Wang et al. 2020). It
has been documented that the level of resistance can be affected by environmental
conditions (Baudouin et al. 2009). In some cases, it has been observed that
resistance depends on environmental factors than genetic as the speculated
resistant cultivars were infected in some regions, while on the other hand they
were resistant in some other regions (Mpunami et al. 1999; Mpunami et al. 2002). In addition, a
palm resistant to some strains will be likely threatened by a different group
and subgroup of phytoplasma even by a new vector when planted in a new region (Odewale et al.
2012).
Information about the rate of mutations in phytoplasma
is scarce due to the difficulty to culture these pathogens. In addition, no evidence is available on the effects of
transmission or vectors on mutations in phytoplasmas. On the other hand, a
study has shown that an induced mutation in the onion yellowing phytoplasma
resulted in the loss of transmission ability of its insect vector compared to
the wild type (Oshima et al. 2004).
There are several virulence factors in
phytoplasmas including SAP11, SAP54, PHYL1 and TENGU, which can induce specific
symptoms in the diseased plants. It has been shown that a mutation in the
virulence factor TENGU resulted in plant resistance to insect vectors. The
mutant phytoplasma could not change the color of the leaves and with such
symptoms, the vectors were not attracted to the plants (Sugio et al.
2014). However, there is no documented literature on the effects of mutations
in virulence factors on the breakdown of resistance.
Transmission trials with insect vectors are more
reliable and real for resistance screening, though a distinction between
resistance to the vector or the phytoplasma is so difficult (Jarausch et al.
2013). In this way, the population dynamics of the vector needs to be
monitored. To test resistance in coconut, researchers test different varieties
in which LYD is endemic (Baudouin et al. 2009; Odewale and Okoye 2013).
To search for resistant varieties, the researchers plant
a range of resistant varieties in any growing area. Such a method is used to make
plant adaptation to the phytoplasma or vector population. However, after a
period, the resistance may breakdown, and symptoms of the disease appear (Quaicoe et al.
2009). Variety evaluation and improvements should be carried out in the
area as resistance has a degree of site-specificity, which may be affected by
environmental factors, especially drought and poor soil conditions, and genetic
variation between phytoplasma populations (Odewale et al. 2012). Adaption in
phytoplasma may occur fast due to repetitive genomes and short time generation.
Gene stacking has been newly suggested in order to stop resistance breaking
down; however, no published work is available on the use
of gene stacking to manage phytoplasmas in palms. CRISPR (Cluster
Regulatory Interspaced Short Palindromic Repeats) is the newest tool for gene
editing (Abdelrahman et al. 2018; Ipoutcha et al.
2019). By this method, phytoplasma resistance traits can be easily known
and exploited for by gene silencing or insertion (Belhaj et al. 2013).
The most important challenge in host plant resistance in
LYD management might be that such resistance to phytoplasma pathogen may change
the susceptibility to other pathogens or pests. For instance, the resistance
cultivars in PNG became more susceptible to two pests, including black palm
weevil Rhynocophorus bilineatus (Montr.) and Oryctes rhinoceros
(Ovasuru 1994).
Despite the challenges mentioned, such an approach was
used in LYD management. For example, CSPWD (Cape Saint Paul Wilt Disease) was
controlled using a hybrid of Vanuata Tall, and Sri Lanka Green Dwarf in Ghana (Quaicoe et al.
2009). Also, Jamaican farmers replaced the Maypan and Malayan dwarf
varieties by a tall variety, which resulted in retrieval of the coconut
industry (Harrison et al. 2002a).
Although replanting the cultivars may be costly and
practical, this method can help the coconut industry as the average age of many
plants in many parts is old. However, the long period, in which coconut last
for sufficient production should be considered (Danyo
2011; Snaddon et al. 2013).
Antibiotic
treatment
Using
antibiotics can prevent or control phytoplasma infection in individual host
plants (Tanno
et al. 2018; Bogoutdinov et al.
2019). To get better results, antibiotics must be used bi-weekly for
four months by systemic treatment. This method is costly and cannot be used in
commercial production; however, it can be applied for beneficial and decorative
palms in hotels or tourist sites (Eziashi and
Omamor 2010). However, the use of antibiotics is forbidden in developed
countries (Musetti et al. 2013). Because of the perceived health risks and
cost of this approach, antibiotics can be used to protect cherished ornamental
trees but have never been considered as a continuous way of management (Been 1995).
Effect of
Abiotic factors and climate change on LYD
Little
relative information is available on how LYD may be affected by abiotic factor.
It was well known that moisture and temperature can affect the severity of
associated phytoplasma (Krishnareddy 2013).
As demonstrated in some studies, disruption in stomata can contribute to
excessive water loss and leaflet flaccidity in palm root wilt (Rajagopal et
al. 1986). Mulches and the density of host plants and the distance
between coconut plantations could affect vector biology and ecology. The spread
of LYD can be affected by landscape and climate (Mora-Aguillera
2002). Researches on “flavescene doreé” and chrysanthemum yellows
revealed that multiplication in insects was faster under cooler with a low CO2
concentration condition (18–22°C; CO2 400); contrary to plants (22–26°C; 800 ppm)
(Galetto
et al. 2011).
The establishment and spread of the phytoplasma vectors
and associated phytoplasma might change due to climate change (Krishnareddy 2013). One centigrade increase in
temperature resulted in shifting ecological zone by up to 160 km, as stated by Thuiller (2007). It has been known that an
increase in temperature may result in insect species spread into new areas and
even new countries (Parmesan and Yohe 2003).
Transmission success may be increased by higher feeding
frequency or faster multiplication in the host due to an increase in
temperature, which may increase the rate of spread of the phytoplasma (Maggi et al.
2014). In the case of LYD, it is so difficult to predict the
consequences of climate change accurately due to lacking the information of the
temperature range of LYDs. Halbert et al. (2014) demonstrated that
LYD phytoplasma could overwinter consistently further north (N29°), therefore
the LYD spread depends on insect physiology rather than ecology.
Conclusion
Phytoplasma
diseases of palms are economically destructive diseases, which have resulted in
significant effects on humans’ economy and nutrition. There are many gaps in
understanding the phytoplasma diseases of palms, including epidemiology,
biology of the phytoplasmas, ecology and the biology of the vector, and the
relationship between the hosts, vector and pathogen. This question opens a
window for further investigation. Vectors play a crucial role in epidemiology.
However, vertical transmission of phytoplasma in plant hosts has been
confirmed. Proper quarantine and seed movement policies are needed to prevent
disease spread. Although many attempts have been ongoing for the identification
of the vectors species, little information is still available. It should be
noted that a transmission trial to confirm a vector is logistically
challenging. In disease management, early detection of the disease and vector
can help implement the best approaches and prevent disease spread. This issue
has been solved by recent quick techniques in detection such as Polymerase
Chain Reaction (PCR), Loop-mediated isothermal amplification (LAMP), and
digital PCR (dPCR).
Acknowledgments
Authors
would like to thank Sultan Qaboos University and VALE Oman for financial
support of the phytoplasma studies.
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