Two and a half billion times per day a human hand reaches for a fresh cup of coffee.
Although arguably dispensable for life per se, with an industry value of US$174 billion,
coffee provides the lifeblood that sustains economies of producing countries located
in the “coffee belt” situated between the Tropics of Cancer and Capricorn. As a “solvent”
in which many human interactions take place, coffee is witness to the broad spectrum
of human activities from the mundane to the pleasurable and personal. However, in
opposition to its economic, cultural, and physiological importance, diseases such
as coffee rust (caused by the fungus Hemileia vastatrix) dictate activity on stock
markets with their periodic epidemics, which in turn affects the migration patterns
of displaced farm workers . Other diseases, such as those caused by coffee ringspot
virus (CoRSV), currently fly mostly under the radar of many integrated pest management
systems. The unique biology of this and related viruses offers exciting research opportunities
ranging from cell biology, plant pathology and physiology, conservation ecology, to
climate change-related epidemiology. This review highlights important aspects of CoRSV,
including its unique features, and examines the potential role of climate change in
its emergence (Fig 1).
Diverse array of research projects related to understanding the effect of CoRSV on
(A) Whether enjoyed alone or in the company of others, coffee is an integral component
of daily life in all countries around the world. Only one small-scale study has been
done to determine the effect of CoRSV on coffee quality . (B) The effect of CoRSV
on the yield of coffee plants has not been examined. (C) No formal investigations
have been made to determine how CoRSV influences the development of coffee cherries.
(D) Only one study has investigated the population structure of CoRSV [8, 35]. It
remains to be determined if phylogenetic trees derived from different CoRSV genes
or from viral RNA isolated from plants or mites are congruent. Furthermore, evidence
for recombination or reassortment of CoRSV genomes has not been investigated in detail.
(E) The reservoir of CoRSV in wild species, particularly in the Cerrado of Brazil,
has not been investigated. It is unknown if the population structure of CoRSV in the
wild is similar to that in coffee plants. (F) The molecular basis for temperature
dependent susceptibility to systemic infections has not been determined . (G)
The cell biology of CoRSV beyond generation of protein interaction and localization
maps is poorly characterized, particularly with respect to identification of host
factors required for replication and cell-to-cell movement, viroplasm formation, and
nucleocytoplasmic trafficking of CoRSV nucleocapsids and proteins . CoRSV, coffee
ringspot virus; NPC, nuclear pore complex; VP, viroplasm; XPO1, Exportin 1.
CoRSV: Its genome organization and occurrence
In contrast to the members of the Nucleorhabdovirus genus (Mononegavirales) to which
they are most closely related , members of the Dichorhavirus genus have bipartite
genomes, although their coding capacity is about the same as that of the plant-adapted
rhabdoviruses (approzimately 14 kb) . All dichorhaviruses are transmitted by species
of false spider mite, Brevipalpus spp., with orchid fleck virus (OFV) being the type
species [3, 4](Fig 2).
Genome organization of plant-adpated negative-strand RNA viruses.
Colors represent proteins of similar function. Each open reading-frame is flanked
by a conserved gene junction (black circle). Gene junctions lacking transcription
start sites are located between the polymerase gene and trailer RNA regions. Note:
“Y” is a standardized notation used here to denote movement proteins. (A) PYDV. Type
species of the genus Nucleorhabdovirus. (B) CoRSV. Genus Dichorhavirus, which have
bipartite genomes. Beneath the genome maps are overlays of single-plane confocal micrographs
of virus-infected nuclei in leaf epidermal cells of transgenic N. benthamiana plants
expressing GFP targeted to endomembranes (green). Nuclei were stained with DAPI to
visualize chromatin (blue). (C) Mock. shown on left of virus-infected nuclei. Nuclei
in virus-free cells have a clearly defined nuclear envelopes, with nuclei being approximately
10 μm at midsection. Scale is 5 μm. (D) CoRSV. Nuclei in these cells contain large
viroplasms that exclude DAPI staining. However, the nuclear envelope is largely intact.
Note that virus-infected nuclei are larger than virus-free nuclei. CoRSV, coffee ringspot
virus; DAPI, 4′,6-diamidino-2-phenylindole; GFP, green fluorescent protein; ldr, leader;
ORF, open reading frame; PYDV, potato yellow dwarf virus; trl, trailer.
CoRSV shares a pattern of emergence observed with numerous other plant viruses in
being described decades ago and then rising into prominence as cultural and environmental
conditions conducive to range expansion of their vectors are met with increasing frequency
[5, 6]. First documented in 1938 , CoRSV is now established over the majority of
coffee growing regions in Brazil . A survey of some of these regions found CoRSV
on 100% (n = 45) of the farms visited. Although the incidence of CoRSV varied greatly
from farm to farm, the ease by which the virus could be found at every location was
a significant and surprising finding.
Phylogenetic analyses of the N gene in 45 CoRSV samples were conducted in order to
provide insight into the population structure of this virus within and between farms
. These studies revealed a strong geospatial relationship among isolates, given
that the genetic distance between any two isolates was a function of the distance
between collections sites. These data support the hypothesis that the spread of CoRSV
is constrained by expansion of populations of Brevipalpus, which exist as haploidized
females due to commensal interaction with Cardinium spp. This fascinating biology
makes this arthropod an exciting subject for phylogeography studies in its own right
beyond its impact as an agricultural pest .
An important and much under-investigated area in CoRSV research is identification
of its wild reservoir hosts. Much of the coffee growing regions of Brazil are surrounded
by wild and semiwild sections of the Cerrado [10–13], a tropical savannah in which
the flora have not been extensively indexed for viruses, despite the ease with which
plants in this region can be found with virus-like symptoms (Fig 1). Given the range
of experimental hosts of CoRSV, it stands to reason that plants in the Cerrado may
serve as reservoir species for CoRSV [8, 14]. Current virus-discovery-by-sequencing
methods [15–17] are ideally suited to mapping the virus population structure of the
Cerrado, which is the second largest savannah ecosystem in the world, with exceedingly
rich biodiversity—much of which is undescribed—and under threat from human activity
Is there evidence for reassortment and recombination of the CoRSV genome?
That the genome of CoRSV, which in all other aspects resembles that of rhabdoviruses
with monopartite genomes, evolved a bipartite organization begs the question whether
this occurred due to the genetic constraints imposed by its unique vector. A bipartite
genome may allow for increased opportunities for reassortment, if not recombination.
Further, phylogenetic investigations based on whole genome and genes other than the
nucleocapsid are required to provide a detailed phylogeography of this virus and its
vector [18–21]. Given the low genetic diversity observed and the strong geospatial
relationship between isolates, it might be expected that the phylogenetic trees derived
from different CoRSV genes would be congruent (Fig 1). Although reassortment of CoRSV
genomic segments has not been determined, it is clear that this mechanism for exchange
of genetic material is possible in dichorhaviruses, based on investigations with OFV
What is the molecular basis for temperature-dependent susceptibility to CoRSV?
Some plant hosts, Chenopodium quinoa and Nicotiana benthamiana, for example, exhibit
a dramatic temperature-dependent susceptibility to CoRSV . In experiments conducted
with both species, plants must be incubated at 28°C for at least five days in order
for CoRSV to establish systemic infections. That this phenomenon occurs in two genetically
dissimilar plant species suggests that the temperature-dependence affects some virus-specific
process. The 2 to 4°C increase in ambient temperatures projected by climate change
predictions may severely impact the occurrence of this virus in reservoir species,
which in turn may impact the severity and frequency of CoRSV in coffee production
New resources required to support CoRSV research
Infection of plant cells by dichorhaviruses, or the related nucleorhabdoviruses, results
in dramatic modification of nuclei without triggering programmed cell death or rendering
nuclei nonfunctional (Fig 2). A number of new resources are required to gain insight
into the molecular events that underlie CoRSV–plant interactions. Most important among
these is the ability to recover infectious virus entirely from complementary DNA (cDNA)
clones, as has been accomplished for sonchus yellow net virus (SYNV), after decades
of sustained efforts . Improved cloning strategies are effective for facile construction
of infectious clones of rhabdoviruses and viruses with long RNA genome such as potyviruses.
Such approaches should be applicable to a broad diversity of virus types , including
Although recombinant systems will facilitate mechanistic studies of functional domains
in viral RNAs and protein, the study of plant nucleotrophic viruses will be advanced
substantially with a more detailed characterization of plant cell nuclei . With
the dramatic remodelling of nuclei by plant-adapted negative-strand RNA viruses, an
essential area that is presently understudied is the characterization of protein dynamics
in response to virus infection. Characterization of the portion of the plant proteome
that associates with, or is resident in, nuclei lags behind that of yeast and mammalian
systems. However, in a screen for novel nuclear proteins, the Goodin lab has identified
several candidate proteins that will provide vital markers for mapping the response
of nuclei to infection by CoRSV and related viruses . As each of the plant-adapted
negative strand RNA viruses examined to date has a unique protein interaction and
localization map , it is anticipated that it will require investigation of a spectrum
of viruses to identify common and unique features of plant–virus interactions. Several
nucleorhabdoviruses and CoRSV can be studied in the common host N. benthamiana, for
which genomics, biochemistry, and cell biology resources are rapidly expanding .
CoRSV has the additional advantage given that it has been shown to replicate in the
model plant Arabidopsis thaliana .
Is CoRSV trying to tell us something?
For the foreseeable future, coffee will remain “the best part of waking up” and all
that follows thereafter in the spectrum of human social activities. That said, climate
change forecasts promise little more than hardships for coffee producers , due
to expansion of the range and prevalence of warm temperature pests such as the coffee
borer , and Brevipalpus mites, the vector of CoRSV, while having a negative impact
on beneficial pollinators critical for high yields . Warmer average temperatures
mean that diseases such as coffee rust will be able to reach higher elevations that
are traditionally relatively free of this disease, a fact certainly vital to organic
Dire predictions aside, it is safe to say that no one associated with any part of
the coffee industry, from grower to barista, is ready to capitulate to forecasts relating
to climate change. To the contrary, the “Third Wave” of coffee is delivering a rapidly
expanding diversity of specialty coffees to the world, and coffee-producing areas
are taking on a regional and/or terroir aspect long associated with wine, as consumers
increasingly relish the nuanced variation that microclimates have on coffee quality,
aromas, and flavor, in addition to increasing interest in the geography and personal
well-being of coffee growers per se. The dire outcomes of climate change on coffee
production specifically, and agriculture in general, may not manifest themselves if
governments of the world exercise the necessary interventions . Otherwise, that
“last drop” of coffee may be realized.