Seed Transmission in the Potyviridae

Abstract

Viral pathogens comprise approximately half of the emerging diseases in plants, and plant introductions (including the international movement of seed) are considered to be one of the most important contributing factors to the emergence of these pathogens. For the most part plant viruses are incapable of surviving outside of host tissue making their long-term propagation dependent on their hosts. Thus infected seeds are an effective strategy that not only allows for pathogen survival from one season to the next, but also for their dispersal. The Potyviridae, as the largest plant virus family, is often considered to be the most economically important and its members rank among the most successful plant pathogens. Seed transmission within the Potyviridae family is not uncommon, however the exact mechanism of viral entry into the germ line is currently unknown, and the genetic basis of seed transmission has yet to be completely elucidated. Seed transmission rates are influenced by complex interactions among a variety of factors including the host cultivar, the virus isolate, environmental conditions, the timing of infection, vector characteristics, and viral synergism. Seed transmission can have an enormous effect on the epidemiology of crop pathogens due in part to the ecology of plant viruses which are often secondarily disseminated via insect vectors with the effect that extremely low frequencies of seed transmission can result in devastating epidemics. This is compounded by the fact that vertically infected seedlings often do not exhibit symptoms of viral infection. Given the potential for seed transmitted viral pathogens to initiate epidemics, it is vital to understand how seed transmission rates translate into epidemics. In addition, as seed transmission is a means of dispersal for these viral pathogens, effective phytosanitary measures to control the spread of these pathogens are crucial.

Full text

Chapter 1
Seed Transmission in the Potyviridae
Heather E. Simmons and Gary P. Munkvold
Abstract Viral pathogens comprise approximately half of the emerging diseases in
plants, and plant introductions (including the international movement of seed) are
considered to be one of the most important contributing factors to the emergence of
these pathogens. For the most part plant viruses are incapable of surviving outside
of host tissue making their long-term propagation dependent on their hosts. Thus
infected seeds are an effective strategy that not only allows for pathogen survival
from one season to the next, but also for their dispersal. The Potyviridae, as the
largest plant virus family, is often considered to be the most economically impor-
tant and its members rank among the most successful plant pathogens. Seed
transmission within the Potyviridae family is not uncommon, however the exact
mechanism of viral entry into the germ line is currently unknown, and the genetic
basis of seed transmission has yet to be completely elucidated. Seed transmission
rates are influenced by complex interactions among a variety of factors including
the host cultivar, the virus isolate, environmental conditions, the timing of infec-
tion, vector characteristics, and viral synergism. Seed transmission can have an
enormous effect on the epidemiology of crop pathogens due in part to the ecology
of plant viruses which are often secondarily disseminated via insect vectors with the
effect that extremely low frequencies of seed transmission can result in devastating
epidemics. This is compounded by the fact that vertically infected seedlings often
do not exhibit symptoms of viral infection. Given the potential for seed transmitted
viral pathogens to initiate epidemics, it is vital to understand how seed transmission
rates translate into epidemics. In addition, as seed transmission is a means of
dispersal for these viral pathogens, effective phytosanitary measures to control
the spread of these pathogens are crucial.
Keywords Epidemiology • Seed infection • Seed-to-seedling transmission
•Potyviridae • Virus
Given that approximately 90 % of the food crops grown worldwide are propagated
from seed (Maude 1996) it is hardly surprising that seed transmitted pathogens
H.E. Simmons • G.P. Munkvold (*)
Seed Science Center, Iowa State University, Ames, IA 50010, USA
e-mail: munkvold@iastate.edu
©Springer Science+Business Media Dordrecht 2014
M.L. Gullino, G. Munkvold (eds.), Global Perspectives on the Health of Seeds and
Plant Propagation Material, Plant Pathology in the 21st Century 6,
DOI 10.1007/978-94-017-9389-6_1
3

would be a significant concern for both growers and industry alike. Seed transmis-
sion is an effective strategy for pathogens, especially viruses, to maintain their
populations in host plants. In 1972, K.F. Baker wrote, “Seed transmission is now
recognized as the method par excellence by which plant pathogens (a) are intro-
duced into new areas, (b) survive periods when the host is lacking, (c) are selected
and disseminated as host-specific strains, and (d) are distributed through the plant
population as foci of infection” (Baker 1972). Most viruses are unable to survive for
any length of time outside host issue, making long-term perpetuation of viruses
particularly difficult, especially for those that infect annual plants. Seed infection is
an effective mechanism to overcome this, so that the long-term survival of the
pathogen is linked to the host (Stacie-Smith and Hamilton 1988). This mechanism
allows not only for the survival of the pathogen from one season to the next, but also
for the long distance dissemination of the pathogen via infected seed (Albrechtsen
2006). One such example is Wheat streak mosaic virus (WSMV) for which phylo-
genetic studies suggest that the introduction of this virus and its subsequent
distribution within Australia was likely via imported seed (Dwyer et al. 2007).
Approximately 20 % of all plant viruses are seed transmitted (Mink 1993), and it
is believed that approximately one third of plant viruses will eventually be shown to
be seed transmitted (Stacie-Smith and Hamilton 1988). Currently 231 viruses are
believed to be seed transmitted (Sastry 2013), with 13 % of these being members of
the Potyviridae (See Table 1.1 for a list of seed transmitted Potyviridae). Among
the viruses that infect plants the Potyviridae is the largest family, and as a result are
often considered to be the most economically important (Berger 2001). This family,
and in particular the aphid-transmitted members, are among the most successful
plant pathogens (Rybicki and Pietersen 1999). Some of the most important crop
pathogens are members of the Potyviridae, including Bean common mosaic virus
(BCMV), Maize dwarf mosaic virus,Lettuce mosaic virus (LMV), Plum pox virus
(PPV), Potato virus Y (PVY), WSMV, and Zucchini yellow mosaic virus (ZYMV)
(Berger 2001).
The Potyviridae is composed of eight genera: Brambyvirus,Bymovirus,
Ipomovirus,Macluravirus,Poacevirus,Potyvirus,Rymovirus, and Tritimovirus.
In addition, there is one as yet unassigned group, which consists of two viruses
(Spartina mottle virus and Tomato mild mottle virus). These genera have a com-
bined total of 203 species with the Potyvirus group being the largest, comprising
146 members (International Committee on Taxonomy of Viruses, 2012). The
classification is based on shared characteristics; all have positive sense RNA
genomes, all save one (Bymovirus) are monopartite, and they share a gene order
as well as sequence homology. The genomes of all members have a VPg (viral
protein genome-linked) covalently linked to the 50end and a polyadenylated 30end.
They also all share the presence of the distinctive pinwheel inclusion bodies of the
Cylindrical Inclusion (CI) protein. Genera and species are differentiated based on
sequence identity, host range, transmission mode, cytopathology, vector transmis-
sion and antigenic properties (King et al. 2012;Lo
´pez-Moya et al. 2001).
Averaged estimates in the late 1990s of worldwide crop losses due to viruses
were between 1 and 7 % depending on the crop species (Oerke and Dehne 2004).
4 H.E. Simmons and G.P. Munkvold

However the economic impact of individual viral epidemics can be enormous. For
example, yield losses of up to 98.7 % have been reported for WSMV (Edwards and
Mcmullen 1988), and annual losses in Kansas alone due to WSMV have exceeded
$30 million (Jons et al. 1981). PVY yield losses range from 10 % and 80 %
(Valkonen 2007), and the global economic impact of PPV over a 20 year period
is estimated to be 576 million Euros (Cambra et al. 2006). Given the current
increase in emerging pathogens that is occurring these figures are likely to increase.
Emerging viral pathogens are significant and constitute 47 % of emerging diseases
in plants, with plant introductions (including the international movement of seed)
being thought to be one of the most important contributing factors to their
Table 1.1 Seed transmitted Potyviridae, their acronyms, and their important hosts
a
Virus Acronym Important Host (Genus)
Artichoke latent virus ArLV Cynara
Bean common mosaic BCMV Phaseolus,Vigna
Bean yellow mosaic BYMV Lupinus,Vicia,Pisum,Melilotus
Blackeye cowpea mosaic BICM Vigna
Cassia yellow spot CasYSV Cassia
Cowpea aphid-borne Mosaic CABMV Glycine,Phaseolus
Cowpea green vein banding virus CGVBV Phaseolus,Vigna
Desmodium mosaic DesMV Desmodium
Guar symptomless GSLV Cyamopsis
Hippeastrum mosaic HiMV Hippeastrum
Leek yellow stripe LYSV Allium
Lettuce mosaic LMV Lactuca,Senecio
Maize dwarf mosaic MDMV Zea
Mungbean mosaic MbMV Vigna
Onion yellow dwarf OYDV Allium
Papaya ringspot PRSV Carica
Pea seedborne mosaic PSbMV Pisum
Peanut mottle PeMoV Arachis,Glycine,Vigna,Voandzeia
Peanut stripe PStV Arachis,Glycine,Vigna
Plum pox PPV Prunus
Potato Y PVY Solanum
Soybean mosaic SMV Glycine,Lupinus,Phaseolus
Sugarcane mosaic SCMV Zea
Sunflower mosaic SuMV Helianthus
Telfairia mosaic TeMV Telfairia
Tobacco etch TEV Nicotiana,Solanum,Capsicum
Turnip mosaic TuMV Raphanus
Watermelon mosaic WMV Cucumis,Echinocystis
Wheat streak mosaic WSMV Triticum
Zucchini yellow mosaic ZYMV Cucurbita,Ranunculus
Adapted from Singh and Mathur (2004). Data from Mink (1993), Sastry (2013) and Albrechtsen
(2006)
1 Seed Transmission in the Potyviridae 5

emergence (Anderson et al. 2004). Other reasons for this increase include conver-
sion of natural vegetation to agriculture, climate change as well as an expansion in
trade and globalization (Jones 2009). Global warming is likely to affect the rate at
which plant RNA viruses evolve as RNA replication is affected by temperature as
are plant defenses (Elena 2011). In addition, climate change will undoubtedly
influence the geographical distribution of crops and plants in natural ecosystems,
and by extension their pathogens and vectors. Warming trends are expected to
change the distribution, winter survival and spring arrival of insect vectors (Ander-
son et al. 2004), potentially affecting viral epidemics, and this has already been
observed, for example, with Barley yellow mosaic virus (Coakley et al. 1999). The
human population is estimated to reach nine billion by 2050 (Cohen 2003), and the
Food and Agriculture Organization estimates that global food production will need
to increase by 60 % by 2050 (Alexandratos and Bruinsma 2012). As agricultural
intensification is thought to expedite the establishment and spread of emerging
viruses (Elena 2011) it is extremely likely that we will continue to see an increase in
emerging viral pathogens. Given that seed transmission is instrumental in the
epidemiology of viral diseases, as it serves as a means of dispersal, both as seeds
and as an initial source of infection for vector dispersal (Mink 1993), the need to
establish rigorous phytosanitary measures for these viral pathogens will become
increasing important.
1 Mechanisms of Seed Transmission
Although seed transmission within the Potyviridae family is not unusual, the
mechanism by which the virus enters the germ line is currently unknown. However,
two possible routes of embryonic infection have been postulated: direct invasion of
the embryonic tissue after fertilization, or infection of the gametes prior to fertil-
ization, either through the ovules or via pollen. In addition, it has been suggested
that the seed transmission rate may be a sum of both indirect and direct embryotic
invasion (Wang and Maule 1994). Plant viruses differ from animal viruses in the
sense that movement of animal viruses into the cell is via receptor-mediated
mechanisms, with the effect that these viruses can exploit the extracellular envi-
ronment. Plant viruses, in contrast, are restricted to the intracellular compartments
of the host and cell-to-cell movement is regulated by the plasmodesmata (Maule
and Wang 1996). Several viral proteins are involved in cell-to-cell movement and it
is thought that the Coat Protein (CP) binds to the viral RNA and alters the exclusion
size limit of the plasmodesmata. This phenomenon is thought to follow the infec-
tion front and is transient (Heinlein et al. 1995; Oparka et al. 1997). The helper
component protein (HC-Pro) is thought to increase plasmodesmal permeability
(Rojas et al. 1997), and the CI is believed to guide the CP-RNA complex to the
plasmodesmata (Rodriguez-Cerezo et al. 1997). In order for systemic infection to
occur, the virus must enter the vascular tissue. The virus moves from the mesophyll
cells and through a series of cells, which are the perivascular parenchyma, the
6 H.E. Simmons and G.P. Munkvold

phloem parenchyma, the companion cells, and finally into the sieve tube elements
(Astier et al. 2001). In the Potyviridae the CP is necessary for viral movement
within host plant tissues, and it is thought that the HC-Pro functions in aiding the
entry and exit of the virus into and out of the host vascular system (Urcuqui-
Inchima et al. 2001). Viral movement through the plant is directed in the sense
that it moves with the carbon metabolites that are transported from the source leaves
to the sink immature leaves; in other words, viral movement follows the same path
as the photoassimilates (Maule and Wang 1996).
The viral genetic basis of seed transmission has yet to be completely determined;
however it appears that a number of viral genes are involved in seed transmission.
Chimeras of transmissible and nontransmissible strains of Pea seedborne mosaic
virus (PSbMV) revealed that the 50untranslated region (UTR), the HC-Pro and the
CP region of the potyvirus genome may be involved in the seed transmission of this
virus (Johansen et al. 1996). The CI may also be involved in seed transmission and
in PSbMV infections; cylindrical inclusions were observed over plasmodesmatal
openings at the testa-endosperm boundary wall (Roberts et al. 2003). Notably all of
the proteins thought to be involved in seed transmission are also involved in viral
movement save one (the 50UTR). When considering seed transmission, the mode of
virus movement within the plant will have an enormous effect on the potential for
vertical transmission, and phloem limited viruses are generally not seed transmis-
sible (Mink 1993).
Evidence for the direct invasion of the embryo is derived from work with
PSbMV. There is some evidence in PSbMV that the virus uses the suspensor as a
mode of entry into the embryonic tissues. After fertilization, the zygote undergoes
an asymmetrical cell division, resulting in a small apical cell, which will become
the embryo and a larger basal cell (the suspensor). In pea the suspensor provides
nutrients for the growing embryo from the endosperm and appears to be anchored
close to the micropyle (a tiny opening in the ovule through which the pollen tube
enters) during the early stages of seed development (Wang and Maule 1994). It is
believed that embryonic invasion occurs as a result of viral movement from the
maternal cells in the micropyle to the endospermic cytoplasm and embryonic
suspensor from where it invades the embryo (Roberts et al. 2003). Given that the
embryonic suspensor undergoes a programmed cell death, the ability of the virus to
gain entry into the embryo in this manner is transient (Wang and Maule 1994), and
thus it appears that seed transmission of viral pathogens in this manner is dependent
at least partially on timing and/or chance (Roberts et al. 2003).
Seed infection can occur via pollen although the frequency of transmission to
seedlings through pollen is generally thought to be less than through the ovules
(Mink 1993). Evidence for the indirect invasion of the embryo via the ovules is
fairly extensive and has been demonstrated for viruses in families other than the
Potyviridae (e.g., Tobacco ringspot virus (Secoviridae) (Yang and Hamilton 1974),
Barley stripe mosaic virus (Vigraviridae) (Carroll and Mayhew 1976), Cucumber
Mosaic virus (Bromoviridae) (Yang et al. 1997), and Turnip yellow mosaic
(Tymoviridae) (de Assis Filho and Sherwood 2000). With respect to the Potyviridae
the evidence for seed transmission via the ovules is substantially less than for other
1 Seed Transmission in the Potyviridae 7

viral families and in some instances is contradictory, for example, in LMV, there
are studies indicating that the seed transmission of this virus does occur through the
ovules (Ryder 1964), and others reporting that it does not (Hunter and Bowyer
1994). However there is some evidence of indirect invasion via pollen in a number
of Potyviridae members, for example, in LMV (Hunter and Bowyer 1997; Ryder
1964) using electron microscopy and immunogold labeling LMV was found to
infect the pollen mother cells (Hunter and Bowyer 1997). Serological work with
PSbMV revealed that the virus was present in pollen in seed transmissible variants
but was absent from these tissues in non seed transmissible isolates (Kohnen
et al. 1995). For some viruses, such as BCMV, there is evidence that direct invasion
of the embryo may occur through both the pollen and the ovules (Schippers 1963;
Medina and Grogan 1961). The seed to seedling transmission rate of Sugarcane
mosaic virus (SCMV) is postulated to be a sum of the direct invasion of the embryo
and indirect invasion of infected pollen. The overall seed to seedling transmission
rate of SCMV in maize was determined to be 4.81 % and the rate of transmission as
a result of infected pollen grains was 0.04–0.10 % (Li et al. 2007).
There is a distinction between viruses that infect the embryo versus those that are
found in other seed tissues or remain as contaminants on the seed surface. This is
significant because embryo infection can readily result in seedling infection while
viral infection of other seed parts will only result in seedling infection if the virus is
easily transmitted mechanically and is resistant to inactivation. Viruses present on
or near the seed surface are often eliminated by heat or chemical treatments and this
is in direct contrast to embryonic infection where the treatments to inactivate the
virus would potentially also kill the embryo (Stacie-Smith and Hamilton 1988).
Seed transmission as a result of the virus being carried on the seed surface is fairly
uncommon (Johansen et al. 1994) and has not been demonstrated in the
Potyviridae. Examples of this mode of transmission include members of the
tabomoviruses, with the only outside member being Southern bean mosaic virus
(Sobemovirus). It would thus appear that the bulk of viruses that are seed-
transmitted are carried within the embryo (Albrechtsen 2006).
2 Factors That Influence Seed Transmission
There are a number of factors that influence seed transmission rates and these
include the host cultivar, the virus isolate, interactions with the environment, the
timing of infection and viral synergism. It has been postulated that whether or not
seed transmission occurs is primarily affected by host-virus interactions and the
timing of infection with environment playing a lesser role (Mink 1993). In addition,
the relation of the virus to its vector may have an effect on seed transmission and
viruses that are horizontally transmitted in a persistent manner are typically not
seed transmitted whereas those transmitted nonpersistently tend to be seed trans-
mitted (Bennett 1969).
8 H.E. Simmons and G.P. Munkvold

Different cultivars within a species can vary in their seed transmission rates. For
instance, using LMV the incidence of seed transmission ranged from 1 % to 8 %
depending on the variety of lettuce (Grogan and Bardin 1950). Similarly an
investigation of seed transmission of PSbMV in 38 pea cultivars revealed that
five of these exhibited no seed transmission whatsoever (Stevenson and Hagedorn
1973). This varietal variation in seed transmission may have a genetic basis and in
soybean seed transmission of Soybean mosaic virus (SMV) appears to be a poly-
genic trait and a number of genes are necessary for high rates of transmission
(Domier et al. 2011). Transmission of different isolates of the same virus can also
vary within a single host. For instance work with Peanut mottle mosaic virus
(PeMoV) revealed differences in the frequency of seed transmission as a function
of virus isolate (Adams and Kuhn 1977). Similarly within PSbMV there are both
transmissible and nontransmissible isolates (Roberts et al. 2003). An investigation
of 14 bean cultivars and four virus isolates showed that seed transmission of BCMV
was influenced by both isolate strain as well as the host cultivar (Morales and
Castano 1987). Seed transmission rates may also be influenced by the interaction of
host cultivar and virus isolate. An investigation of eight soybean cultivars and seven
SMV isolates (Tu 1989) found that the interaction between host cultivar and virus
isolate resulted in the seed transmission rate varying from zero to 70 %; a resistant
cultivar had overall lower seed transmission than the susceptible cultivar, but at
least one SMV strain was seed-transmitted at a higher rate in the resistant cultivar.
The environment can affect seed transmission rates and studies using SMV
elucidated that temperature had an effect on seed transmission in soybean.
Although virus symptoms on the mother plants were most severe when plants
were grown at 25 C, seed transmission was optimal when the plants were grown
at 20 C (average 48 %) and seed transmission decreased at 15 C (average 7 %)
and 25 C (average 9.7 %) (Tu 1992). Work with PSbMV determined that reduced
rainfall decreased the incidence of virus in the field because it resulted in a delay of
the vector (Coutts et al. 2009). Thus the risk associated with a given level of seed
infection was dependent on conditions before and after planting. It is apparent that
the factors influencing seed transmission rates are complex, as suggested by Maule
and Wang (1996), and are the result of multifaceted interactions between the host,
virus, vector and environment.
The seed transmission rate can be greatly influenced by the age of the host
(flowering) at the time of inoculation. Seed transmission rates appear to be
inversely related to the age of the plant (and/or developmental stage) upon infection
(Wang and Maule 1992). In SMV a reduction in seed transmission of 13 % (16–
3 %) was seen after the onset of flowering (Bowers and Goodman 1979). Likewise
the date of inoculation was seen to influence the incidence of seed transmission in
BCMV with the effect that seed transmission increased significantly if inoculation
occurred within the first 20 days of the vegetative period of the host. In the same
study, only 2 of 14 bean cultivars exhibited seed transmission if inoculation
occurred more than 30 days after sowing (Morales and Castano 1987). Other
Potyviridae for which the age of the host appears to affect seed transmission rates
1 Seed Transmission in the Potyviridae 9

include PSbMV (Wang and Maule 1992), BCMV (Kaiser and Mossaheb 1974) and
PeMoV (Paguio and Kuhn 1974).
Synergism can affect seed transmission rates although the direction of influence
appears to vary, for instance, co-infections of PSbMV with Pea early browning
virus (PEBV) (Virgaviridae) resulted in seed transmission being blocked in PSbMV
although it was unaffected in PEBV (Wang and Maule 1997). For viruses in other
families a synergistic effect that increases the rate of seed transmission has been
reported e.g. Turnip yellow mosaic virus (Tymoviridae) (de Assis Filho and
Sherwood 2000), and Southern bean mosaic virus (Sobemovirus) (Kuhn and
Dawson 1973).
3 Seed to Seedling Transmission
Although the majority of seed transmission events require embryonic infection,
embryo infection itself does not necessarily result in seedling infection. In fact the
discrepancy between seed infection rates and seed to seedling transmission rates
can vary greatly. For instance in ZYMV the seed infection rate was significantly
higher (21.9 %) than the seed to seedling transmission rate (1.8 %) (Simmons
et al. 2013). Similar results were found with LMV (Hunter and Bowyer 1993).
However, there are instances where the whole seed-assay matches up with the seed
transmission rate, for example in SMV (Bowers and Goodman 1979) and Peanut
stripe virus (Xu et al. 1991), but this does not appear to be the norm (Albrechtsen
2006). One possible explanation for this is that inactivated viruses can occur in parts
of the seed other than the embryo, with the effect that the virus is still detectable via
serological or molecular methods. In these instances testing the whole seed for the
virus will lead to an overestimation of the actual seed transmission rate. For viruses
that infect the embryo, the seed to seedling infection rate is going to be the result of
two factors: the first is the ability of the virus to survive in the embryo, and the
second is its ability to be reactivated (Albrechtsen 2006). It is believed that a virus
that has infected the embryo will remain viable for as long as the seed is viable
(Bennett 1969) and there are examples of extreme longevity of seeds and their
pathogens; BCMV has been shown to be able to survive and remain infectious for
30 years in seed (Pierce and Hungerford 1929).
Symptoms in seedlings are variable and appear to be dependent on the virus
strain, host genotype and environment (Albrechtsen 2006). For example, with
BCMV in some seedlings, viral symptoms did not appear until the second or
third trifoliate leaf (Kaiser and Mossaheb 1974). Vertically infected seedlings
often exhibit little to no symptoms of viral infection (Stacie-Smith and Hamilton
1988), and as a result visual inspection is frequently not the optimal method for
determining the incidence of seed transmission for these pathogens. Cucurbit
seedlings vertically infected with ZYMV demonstrated little to no visual symptoms
(Simmons et al. 2013; Muller et al. 2006; Gleason and Provvidenti 1990), while
slight symptoms have been observed in PSbMV (Hampton 1972). There may be a
10 H.E. Simmons and G.P. Munkvold

genetic basis for this and Illumina sequencing of ZYMV populations revealed that
the 50UTR is highly variable in the seed transmitted populations compared to those
transmitted horizontally. In this example the vertically transmitted populations
were symptomless in comparison to the horizontally transmitted populations
(Simmons et al. 2013). Likewise, studies with PPV determined that a deletion in
this region resulted in reduced symptom development (Simon-Buela et al. 1997)
and in BCMV an insertion in this region resulted in an increase in symptom severity
(Zheng et al. 2002).
For some members of the Potyviridae the presence of the virus in the seed does
not appear to affect germination rates, for instance in PSbMV (Hampton 1972), and
in BCMV (Raizada et al. 1990; Hao et al. 2003). For others, however, there does
appear to be an interaction between seed infection and low germination rate. This
could potentially lessen the effect of epidemics, as only a subset of virally infected
seeds will successfully initiate infections in subsequent generations. For instance in
ZYMV the germination rate of seeds extracted from fruits from infected parents
was 22.5 % versus 87.5 % for those harvested from non-infected parents (Simmons
et al. 2013). This could be due to a number of reasons. It is possible that the lower
germination rate could be the result of the effects of the pathogen on the mother
plant, or the virus could be reducing the viability of the seed. This was found with
SMV where infection severely reduced the seed yield. Viral infection reduced seed
yield on average 58.5 % among eight soybean cultivars inoculated with seven virus
isolates (Tu 1989). Similarly low numbers of viable seed were reported from
ZYMV infected plants (Desbiez and Lecoq 1997). It is also possible that the viral
titers in the seeds are simply too low to consistently initiate effective infections in
the subsequent generation. A determination of viral titers via qPCR revealed that
the titers of ZYMV were several orders of magnitude lower in the seed (11.3–
60 ng/μl) than in the leaf (2,000–3,400 ng/μl) (Simmons et al. 2013). Alternatively,
the viral population may be severely constrained by the host plant such that only a
subset of the viral population is transmitted from the seed to the seedling, or host
defense mechanisms, such as RNA silencing, may be eliminating the viral popula-
tion, or preventing it from being transmitted to the seedling. An investigation of the
numbers of infectious PSbMV particles that were subsequently transmitted to a
vertically infected seedling from the mother plant was on average only one,
suggesting that the bottleneck for this mode of transmission is very severe indeed
(Fabre et al. 2014).
The ecology of plant viruses is such that seed transmission can have an enor-
mous effect on the epidemiology of crop pathogens. This is due to the fact that the
majority of plant viruses are secondarily disseminated via insect vectors; therefore
small initial numbers of infected plants can lead to damaging epidemics (Maule and
Wang 1996). This is particularly important as many of the plant viral vectors
transmit nonpersistently, which means that insecticides are not effective at
suppressing secondary spread. This is due to the fact that both acquisition and
inoculation occur rapidly (within a few seconds), and thus the vector is not exposed
for a sufficiently long enough period of time for the pesticide to be effective in
reducing viral spread. As a result, the vector can often spread the virus to a
1 Seed Transmission in the Potyviridae 11

neighboring plant before it is negatively affected by an insecticide (Perring
et al. 1999). In addition the frequency at which seed transmission occurs may not
be a good predictor of the epidemiological significance of a virus, and even
extremely low transmission rates can initiate severe epidemics. For example
LMV at an incidence of 0.001 resulted in an epidemic as a result of secondary
spread via the insect vector (Ryder 1973). Similarly PeMoV at a seed transmission
of 0.1 % is sufficient in the epidemiology of this pathogen (Adams and Kuhn 1977).
Given the potential for seed transmitted viral pathogens to initiate epidemics and
the fact that viral pathogens are the most abundant group of emerging pathogens in
plants, it is vital to understand how seed transmission rates translate into epidemics.
There has been a lack of research examining the relationship between seed infection
levels on the development of viral epidemics and the resulting risk to crop yields.
This is vitally important for informing both seed industry as well as farmers (Jones
2000). Except for a few notable Potyviridae examples such as PSbMV, where
research resulted in a threshold value of >0.5 % seed infection (Coutts
et al. 2009), and LMV, for which a threshold of 0.1 % was established (Tomlinson
1962; Zink et al. 1956) very little quantitative work has been performed in this area.
Although not Potyviridae members an excellent example of determining threshold
levels was undertaken with two Bromoviridae (Cucumber mosaic virus and Alfalfa
mosaic virus). This study underscores the necessity of determining threshold levels
that are based on an examination of particular host-virus interactions, specific
geographic sites as well as year-to-year variations (Jones 2000). Given that differ-
ent viral pathogens will have different thresholds it is critical that this type of
research be conducted on individual virus-host pathosystems, as generalities cannot
be applied to specific cases.
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