Human Pathogens on Plants:
Designing a Multidisciplinary Strategy for Research
Jacqueline Fletcher, Jan E. Leach, Kellye Eversole, and Robert Tauxe
First author: National Institute for Microbial Forensics & Food and Agricultural Biosecurity, Department of Entomology & Plant Pathology,
Oklahoma State University, Stillwater, OK; second author: Bioagricultural Sciences and Pest Management, Colorado State University, Ft.
Collins, CO; third author: Eversole Associates, Bethesda, MD; and fourth author: Centers for Disease Control & Prevention, Atlanta, GA.
Accepted for publication 29 January 2013.
Fruits and vegetables, often eaten without cooking, are im-
portant in a healthy diet, but they also are implicated increasingly
in outbreaks of foodborne illnesses (54); annual public health
outbreak surveillance has revealed increases in both numbers and
sizes of disease outbreaks over the past several decades (77). The
produce items most often identified in these outbreaks were leafy
greens, melons, sprouts, berries, tomatoes, and green onions, all
of which are likely to be eaten with minimal further processing.
Outbreaks of Shiga toxin-producing Escherichia coli O157:H7
infection linked to lettuce and spinach (38,87); salmonellosis
linked to cantaloupes, tomatoes, and hot peppers (10,14,33,60);
hepatitis A linked to green onions (88); the Shiga toxin-producing
E. coli O104 infections in Germany linked to fenugreek seed
sprouts; and Listeria monocytogenes infections linked to cantaloupe
(17) underline the challenge of fresh produce contamination (see
Corresponding author: J. Fletcher; E-mail address: email@example.com
© 2013 The American Phytopathological Society
Note: Recent efforts to address concerns about microbial contami-
nation of food plants and resulting foodborne illness have prompted
new collaboration and interactions between the scientific com-
munities of plant pathology and food safety. This article provides
perspectives from scientists of both disciplines, and presents
selected research results and concepts that highlight existing and
possible future synergisms for audiences of both disciplines.
Fletcher, J., Leach, J. E., Eversole, K., and Tauxe, R. 2013. Human pathogens on plants: Designing a multidisciplinary strategy for research.
Recent efforts to address concerns about microbial contamination of food plants and resulting foodborne illness have prompted new collaboration
and interactions between the scientific communities of plant pathology and food safety. This article provides perspectives from scientists of both
disciplines and presents selected research results and concepts that highlight existing and possible future synergisms for audiences of both
disciplines. Plant pathology is a complex discipline that encompasses studies of the dissemination, colonization, and infection of plants by microbes
such as bacteria, viruses, fungi, and oomycetes. Plant pathologists study plant diseases as well as host plant defense responses and disease man-
agement strategies with the goal of minimizing disease occurrences and impacts. Repeated outbreaks of human illness attributed to the contami-
nation of fresh produce, nuts and seeds, and other plant-derived foods by human enteric pathogens such as Shiga toxin-producing Escherichia coli
and Salmonella spp. have led some plant pathologists to broaden the application of their science in the past two decades, to address problems of
human pathogens on plants (HPOPs). Food microbiology, which began with the study of microbes that spoil foods and those that are critical to
produce food, now also focuses study on how foods become contaminated with pathogens and how this can be controlled or prevented. Thus, at the
same time, public health researchers and food microbiologists have become more concerned about plant–microbe interactions before and after
harvest. New collaborations are forming between members of the plant pathology and food safety communities, leading to enhanced research
capacity and greater understanding of the issues for which research is needed. The two communities use somewhat different vocabularies and
conceptual models. For example, traditional plant pathology concepts such as the disease triangle and the disease cycle can help to define cross-over
issues that pertain also to HPOP research, and can suggest logical strategies for minimizing the risk of microbial contamination. Continued
interactions and communication among these two disciplinary communities is essential and can be achieved by the creation of an interdisciplinary
research coordination network. We hope that this article, an introduction to the multidisciplinary HPOP arena, will be useful to researchers in many
Vol. 103, No. 4, 2013 307
Glossary for definitions of terms in bold font) occurring in the
field or early in the processing phase. Enteric bacterial patho-
gens, commonly transmitted through foods, like Salmonella,
Shiga toxin-producing E. coli, Shigella, and Campylobacter, are
well adapted to vertebrate hosts and typically colonize the gut.
Some have humans as their primary or sole host, while many
others are sustained in animal populations, are adapted to a
particular reservoir or environment, and affect humans only
incidentally. For example, members of the genus Campylobacter
are adapted to birds, in which they are commensal intestinal flora,
and can transfer to poultry meat at slaughter (85). Some strains
colonize cattle and are transmitted via raw cows’ milk. Shiga
toxin-producing E. coli O157:H7 can colonize the peri-rectal
glands of ruminants and transfer from hides and feces to meat
during the slaughter process (34). Salmonella enterica serotype
Enteritidis can leave the gut to colonize the peri-ovarian tissues of
a hen’s reproductive tract, thereby contaminating the internal
contents of normal appearing eggs (53). The phrase “human
pathogens on plants” (HPOPs) has been proposed recently to
describe such pathogens when they inhabit, colonize, enter, or
otherwise interact with plants.
Interestingly, the Gram negative bacterial family Enterobac-
teriaceae, which includes many of the human pathogens associ-
ated with plant foods (e.g., Escherichia, Salmonella, and Shigella),
also contains a number of genera of plant pathogens (Entero-
bacter, Erwinia, Pantoea, Pectobacterium, etc.) that cause plant
diseases such as blights, wilts, and soft rots. The taxonomic
relatedness of these plant and human pathogens raises interesting
questions about the possibilities for niche competition or syner-
gism, horizontal nucleic acid exchange in protected plant niches,
or even host range expansion. There are microbial species, some-
times referred to as cross-over pathogens, that infect and cause
disease on both plants and humans, though these are relatively
uncommon. Examples of currently recognized cross-kingdom
pathogens include a few bacterial species that commonly inhabit
plant surfaces and the rhizosphere, such as Pseudomonas aerugi-
nosa, Burkholderia cepacia, Dickeya spp., Enterococcus faecalis,
and Serratia marcescens (84).
The plant disease triangle. A central dogma of plant pathol-
ogy known as the disease triangle (Fig. 1) maintains that the
development of a plant disease requires at least three components:
(i) the pathogenic microbe must be virulent on a particular species
and cultivar of plant; (ii) the plant host must be susceptible to a
particular strain/isolate/biotype of a pathogen; and (iii) environ-
mental conditions including temperature, humidity, and avail-
ability of nutrients for the pathogen must be suitable for both
pathogen survival and the interactions that lead to disease. In
cases in which an insect vector is required for pathogen dis-
semination, some plant pathologists have expanded the concept to
that of a disease pyramid with the fourth dimension representing
the insect (this fourth dimension would encompass any other type
of living vector as well). Venn representations of these concepts
(Fig. 1) emphasize that without all three (or four) components
disease will not occur.
The plant disease cycle. A second dogma of plant pathology is
that, although every disease is unique, for a given plant disease
the pathogen, plant, and environment (and insect vector, if in-
volved) interact with one another in generally predictable ways
that can be represented as a disease cycle. The disease cycle is a
holistic picture that summarizes the process within the context of
an environment that includes both natural systems and agricul-
tural inputs. Critical nodes include pathogen overwintering/over-
seasoning, dissemination/ transmission mechanisms, inoculation,
colonization (multiplication), infection and establishment, disease
initiation, symptom development, and pathogen propagule forma-
tion finally closing the cycle. Relevant subcycles and alternative
pathways are often incorporated.
The disease cycle is far more than a device by which to
remember the steps of the disease process, however. Logic tells us
that disease may be hampered or prevented by blocking any step
in the cycle. Thus, each cycle node or pathway is an opportunity
for disease management and a potentially fruitful area for re-
search into best management practices. For example, the plant
pathogenic bacterium Xanthomonas axonopodis pathovar (pv.)
vesicatoria spends much of its life as an ephiphyte on the
surfaces of a variety of plants, living on plant exudates, inter-
acting with other members of the phylloplane microbial com-
munity, and forming colonies protected and facilitated by biofilm
formation (Fig. 2). Only on certain plants in the family Solanaceae,
such as tomatoes and peppers, and only when conditions remain
suitably warm and humid for several days do some bacteria enter
the plant through natural openings such as stomata or through
wounds. Their internal colonization leads to infection and to the
physiological processes that result in the disease known as bac-
terial spot, and to the appearance of characteristic necrotic spot
symptoms on leaves and fruits (Fig. 2; 68).
Affected leaves often abscise and accumulations of bacteria-
laden plant debris and seeds provide inoculum for subsequent
infections. The impact of this disease can be economically
devastating with some growers even plowing under their crops if
disease begins early in the season when a minimal yield appears
certain. The bacterial spot disease cycle (Fig. 2; 68) shows not
only the steps of disease progression but also that disease devel-
opment can be interrupted by strategies that target various nodes.
Although the cycle could begin at any point, for the sake of
simplicity we begin our example with seed contamination (#1 in
Fig. 2), where a farmer could kill bacteria in contaminated seeds
by applying heat or chemical treatments during storage or before
planting. Other strategies to limit damage take advantage of dif-
ferent weak points in the cycle, including (#2 in Fig. 2) removing
potentially infected crop debris from the field after harvest, (#3)
targeting the epiphytic phase of the life cycle, (#4) preventing
Abscise: detach, as a senescing leaf from a stem
Colonization: multiply and establish a physiologic relationship
with a host; may or may not lead to disease
Contamination: presence of undesirable organisms
Enteric: associated with the animal gut
Epiphyte: resident on a plant surface
Endophyte: resident within a plant
HPOP: a human pathogen that can be found in association with
Hydathode: natural plant pore, located at leaf tips and edges,
through which gas exchange and water loss occurs
Infect: establish a physiological relationship with a host leading
Infest: be present on or in
Pathovar (pv.): informal plant-pathogenic bacterium taxon
defined by the plant host range
Phylloplane: the surface of a plant
Propagule: a pathogen life stage, usually asexual, that is
Rhizosphere: the region proximal to a plant’s roots
Serotype: pathogen type defined by serological reactions to
Stomate/stomata: natural plant pores, on leaf, flower and stem
surfaces, through which gas exchange and water loss occurs;
openings regulated by the turgor pressure of guard cells
Trichome: hair-like projection of a leaf epidermal cell
aerial pathogen dispersal, or (#5) treating plants with bactericide
sprays, either at the time of symptom appearance or on a regular
spray schedule during periods when the plant is susceptible and
weather conditions are conducive to disease development.
The involvement of arthropods and other animals (birds, wild
mammals, reptiles, etc.) as vectors of a number of plant patho-
gens, the ample evidence that a variety of insect species move
freely between livestock holdings and produce fields, and the
many reports of human pathogens carried on insect mouthparts,
legs, and wings suggests that studies of HPOP dissemination
within the environment would be incomplete without considera-
tion of the myriad of species that commonly move back and forth
between these agricultural settings (15,23,55,80). Indeed, labora-
tory experiments have shown that blow flies can pick up E. coli
O157:H7 from contaminated manure and deposit them onto the
phylloplane of a number of edible plant species, where the bac-
teria can then colonize and multiply (80). Whether this happens in
nature on a significant level remains unclear.
Can a holistic diagram such as the plant disease cycle be useful
for managing foodborne human pathogens too? Several authors
have represented HPOP–plant interactions and associated factors
(9,15,82) in diagrams reminiscent of a disease cycle, and these
do, in fact, suggest a variety of points for interrupting the process
or reducing human pathogen amplification.
Disease management–plant-pathogenic bacteria. Numerous
plant disease management strategies that are not obvious from the
disease cycle also could be useful when applied to HPOPs.
Cultural practices, such as providing well-drained soils, avoiding
low, frost-prone or water-logged areas, and applying fertilizers
well-matched to a crop species, promote healthy, robust plant
growth and plant defense responses. Identifying and treating
pathogen reservoirs such as contaminated water, soil, or equip-
ment helps eliminate or reduce inoculum the next season. Insects
that can disseminate bacteria and also cause wounds through
which bacteria enter can be controlled through integrated pest
management (IPM) strategies, including judicious application of
appropriately labeled antimicrobials. While partial control of
some plant diseases can be achieved with biological control (i.e.,
the use of benign microbes to occupy plant niches that would
otherwise be available to pathogens, to secrete bacteriocins, or to
out-compete harmful ones for scarce nutritional resources), more
effective biocontrol agents are needed. Finally, we now have plant
cultivars that are resistant to certain plant pathogens. Although
complete immunity is an unreasonable goal, increased resistance
can help keep plant disease levels below an economic threshold.
Can some of these same strategies work also for HPOPs?
Understanding interactions reveals clues for control. Most
of our knowledge of plant–microbe interactions is built on studies
involving plant interactions with plant pathogenic or beneficial
microbes (48,51,52,72). Communications between the plant and
the microbe can occur on the plant surface (epiphytes on leaves,
roots, fruits, or stems) or within the plant (endophytes that colonize
between plant cells or in the vascular system). In other words, the
plant senses the pathogens’ presence, and this recognition can
determine whether the microbe can successfully colonize the
plant or whether the plant mounts a defensive response and
thwarts infection. Recent research, stimulated in part by human
disease outbreaks attributed to plant based foods (nine research
projects were funded in 2007 by a fresh produce company to
address practical questions and find practical solutions to mi-
crobial contamination of fresh produce ) has shown that
human enteric pathogens also can have complicated interactions
HPOPs are usually thought of as having a reservoir in the
intestines of a vertebrate host and, once shed in manure, can come
into direct or indirect contact with produce by various routes.
Thus, historically, they were considered to be transient on plant
surfaces, persisting passively in cracks, wounds, and natural
openings such as stomata or hydathodes (respiratory pores on
plant surfaces or edges, respectively). They were thought incapa-
ble of actively modifying the plant or communicating with it.
However, it is now clear that enteric bacteria don’t just “land” on
and passively inhabit plants. These pathogens can adhere tightly
to produce, multiply, and enter into the tissues of leaves or fruits,
in some cases even moving into other plant parts (12,24). Since
washing food surfaces can remove only part of this contamination
(13), it is particularly important to understand and prevent con-
tamination from happening in the first place (9,62,70,73).
For example, E. coli O157:H7 or Salmonella spp. that contami-
nate alfalfa seeds will multiply rapidly in the young sprouts,
appearing at high counts throughout the young plant (24,53).
Salmonella spp. splashed onto leaves may enter them and spread
via the plant’s vascular system to other edible parts of the plant
(12). Human enteric pathogens have been shown to enter warm
fruits placed in cold water because of internal pressure changes
(30,43,44) and to enter edible plant tissues through bruises and
wounds (64,71). There are recurrent associations between particu-
lar pathogens and particular produce types, e.g., pathogenic E.
coli is more often associated with leafy greens, while Salmonella
sp. is more often associated with tomatoes and cantaloupes. Is this
simply the result of contamination geography and opportunity or
is a more specific specialization present? Once on a plant,
bacteria demonstrate preference for certain niches; on tomato
leaves, S. enterica prefers the shelter of type I trichomes on leaf
surfaces (6). In contrast, on fresh lettuce leaves in the dark
Salmonella cells distribute randomly over the leaf surface, but
when light stimulates photosynthesis, they concentrate at the
stomatal openings (respiratory pores) on the leaf, possibly drawn
The plant disease triangle indicates the three
components necessary for disease to occur. If
a pathogen requires an insect vector for
dissemination or inoculation then a fourth
dimension is added (a plant disease pyramid).
Venn versions of the plant disease triangle and
pyramid emphasize that disease can occur only
at the intersection of all components.
Vol. 103, No. 4, 2013 309
to products of photosynthetic metabolism (47). Some HPOPs, like
some phytopathogenic bacteria, even manipulate the opening or
closing of those stomatal pores by signaling the encircling guard
cells, whose turgor pressure changes control the pore size (16,
47,57,58,72,91). One research group reported that E. coli O157
uses a specific type III secretion system effector to manipulate the
stomatal guard cells of spinach leaves so that they open (72).
Human bacterial pathogens may even spread within a plant during
the reproductive process, as Salmonella spp. placed on the pistil
of a tomato or cantaloupe flower can travel to the ovule and
colonize new fruits as they form there (28,32). Many of these
interactions mimic those of other microbes that have nothing to
do with human illness, but which are well studied by plant pathol-
ogists. The field of plant pathology thus has important contri-
butions to make in understanding the factors involved in microbial
contamination of plant based foods and improving strategies for
minimizing that risk.
As a result of these and other findings, a working hypothesis
emerging among food scientists and plant pathologists is that
adaptation to persist and grow on plants and associated environ-
ments (soil, rhizosphere, etc.) is a natural part of the life cycle for
human pathogens just as it is for plant-pathogenic microbes (73,
82). Like plant pathogens, human pathogens can persist in soil
and in crops for prolonged periods (7,41,42,45,89,90). Some
human pathogens, such as Salmonella spp. and E. coli O157, not
only associate with and colonize plant surfaces, but more alarm-
ing from a food safety perspective, they internalize within the
structure of the plant, though not necessarily within the plants
cells, and live as endophytes within the plants (21). Even more
surprising to the research community was evidence that human
pathogens actively communicate with plants and other plant-
associated microbes during the plant/environment part of their life
cycle (40,73–75). Knowing how human pathogens interact with
plants and what these processes share in common with plant
pathogens provides clues for actively managing HPOPs.
HPOPs and plant pathogens share lifestyle strategies. When
it comes to the genes that are required for survival in the environ-
ment and for interactions with eukaryotic hosts, microbes, regard-
less of whether they are adapted to human or plant hosts, share
many genetic mechanisms. Since human pathogens attach to,
multiply in and colonize plants, and exhibit preferences for tissues,
commonalities with plant pathogens in the mechanisms they use
for colonization of plants would be expected. The nature of the
particular phylloplane environment encountered by any microbe
is a critical element in whether that organism will perish, survive,
or thrive there. The availability of water and nutrients is essential
for colonization and may also contribute to host specialization.
Nutrients are supplied in the form of natural plant exudates, fluids
that leak from wounded plant surfaces or broken trichomes, insect
feces (honeydew), and decaying organic matter (2,83). If a film of
water is present, plant pathogens may display chemotaxis, trans-
locating by means of flagella toward attractive substances or away
Disease cycle of bacterial spot of pepper and tomato, caused by Xanthomonas axonopodis pv. vesicatoria. (Adapted, with permission, from Ritchie
. Images courtesy of Florida Division of Plant Industry Archive, Florida Department of Agriculture and Consumer Services, Bugwood.org
(diseased leaves); Graves, A. S., and Alexander, S. A. 2002. Managing bacterial speck and spot of tomato with acibenzolar-S-methyl in Virginia.
Online. Plant Health Progress doi:10.1094/PHP-2002-0220-01-RS [diseased tomato fruit]; Kawia Scharle/Shutterstock.com [tomato seeds]; Denis
Nata/Shutterstock.com [tomato seedlings]; Jerry Horbert/Shutterstock.com [tomato plants]; J. Bicking/Shutterstock.com [nonhost plants]; and
from repellent ones. For example, Erwinia amylovora, the causal
agent of fire blight of apples and pears, moves toward a variety of
organic acids present on apple leaves (66).
Some genes that affect human pathogen virulence in vertebrates
are also involved in their attachment to and colonization in plants,
though not to cause plant disease (4,5,72). Further, some Salmo-
nella sp. genes, such as those encoding cellulose and O-antigen
capsule seem to be related specifically to colonization of plants
(and not necessarily of vertebrates) (5). An early described ex-
ample of shared strategies was that both plant and human patho-
gens require type III secretion systems (TTSS) to cause disease.
Not surprisingly, when whole genome comparisons among
microbes became feasible, even more commonalities between
human and plant pathogens microbes were revealed. The use of
mutagenesis approaches to characterize the functions of common
genes has shown repeatedly that many are involved in the
production of virulence factors or are required for host invasion
and colonization or adaption to environment-imposed stresses,
and that these are essential for pathogenesis to both plants and
humans (4,5,74,79) Both groups of pathogens produce exopoly-
saccharides that can protect pathogens from desiccation as well as
from host recognition; appendages such as flagella, pili, or in the
case of some HPOPs, coiled, aggregative filaments known as curli
(83), and fimbriae, all of which have roles in co-aggregation and
adherence to host surfaces (81). Siderophores produced by both
groups sequester elemental iron, an essential cofactor in many
host functions (35). Both human and plant pathogens form bio-
films, complex, often multispecies microbial communities that
allow diversification of roles of individual community members
and toxins (3,35,49,50,67). While they may use different mo-
lecular languages for quorum sensing, there is evidence that
human enteric bacteria can perceive signal molecules used by
plant pathogens for regulation of pathogenicity genes (for review,
see Roper  and Smith et al. ). As mentioned above, both
use highly conserved secretion systems, such as TTSS, to deliver
virulence factors to the host surface or inside the host cell
Bacteria that cause illness in both plants and vertebrates may
have genes that contribute to the virulence in both hosts. For
example, Pseudomonas aeruginosa is a particular problem for
children with cystic fibrosis, in whom it causes persistent lung
infections; it also can infect plants and other hosts. Isolates of P.
aeruginosa obtained from ill humans studied by gene deletion
showed two pathogenicity islands, both of which contained genes
for plant and animal virulence. Remarkably, half of the genes
studied contributed to virulence in both hosts (36). Using cross
kingdom models may provide a way to screen for virulence
factors. For example, strains of P. aeruginosa from cystic fibrosis
patients were tested for their ability to invade a wounded alfalfa
seedling. Invasiveness in young plants was associated with a gene
controlling the production of alginate, a factor related to harmful
persistence of certain strains in children with cystic fibrosis (76).
It is important to note that the common tools shared by human
and plant pathogens are not used only for interactions or com-
munications with their hosts. They are also critical components of
their interactions with other microbes in the environment and
within the tissues of either host. For example, biofilms, which are
important in many cases for pathogenesis (3,5,49) and protection
of microbes, are frequently composed of multispecies communi-
ties (20,26,27,61,67). Forming such a community would likely
involve communications among the bacteria within the biofilms
(3,7). It has been speculated that colocalization of human and
plant pathogens within biofilms or within plants may benefit the
less adapted human pathogen (3,7,86). In addition, colocalization
of the microbes would provide opportunities for genetic exchange
among the diverse pathogens; this possibility for transfer of
genetic information is of concern, as traits that improve fitness of
both types of pathogens (antibiotic resistance, etc.) may be ex-
changed. One example is the emergence of streptomycin-resistant
strains of plant pathogens (Erwinia amylovora, Pseudomonas
spp., and Xanthomonas campestris) and the observations that
some of the streptomycin resistance genes in these bacteria are
associated with transfer-proficient mobile elements, and that the
genes are similar to streptomycin resistance genes found in
bacteria isolated from humans, animals, and soil (for review, see
Heuer et al.  and McManus et al. ). The fact that several
important and widely occurring plant pathogens are members of
the family Enterobacteriaceae, closely related to significant
HPOPs, makes interspecies gene transfer even more likely.
Since plant pathogens and human pathogens use several com-
mon mechanisms for infection, colonization, and survival in the
host, strategies that interfere with these processes, used for
controlling plant pathogens, might also control HPOPs. One
approach is to target the quorum sensing communication path-
ways used by the microbes. Several plant pathogenic members of
the family Enterobacteriaceae, including those that colonize
vascular and intercellular spaces, communicate using N-acyl-L-
homoserine lactones (AHLs) that bind to transcriptional regu-
lators and activate or regulate target genes important for plant
colonization (for review, see Crepin et al.  and Roper ).
Human enteric pathogens, such as E. coli and S. enterica, do not
synthesize AHLs, but they do contain an AHL receptor that can
bind AHLs produced by other bacterial species and thereby use
this quorum sensing signal to regulate their own gene transcrip-
tion (for review, see Smith et al. ). By expressing an enzyme
that hydrolyzes the lactone bond of AHLs in tobacco, Dong et al.
(22) interfered with the inter-bacterial communications and sig-
nificantly increased resistance of the tobacco to infection by the
plant-pathogenic Enterobacterium Erwinia carotovora.
Plant genetic resistance. Plants are protected from potential
pathogens by surface barriers (e.g., thick cell walls, waxy cuticle)
or through the activation of innate immune responses (reviewed
by Abramovitch et al. ). The latter are activated by the inter-
action of pathogen-associated molecular pattern (PAMP) molecules
with plant extracellular plasma membrane receptors called pattern
recognition receptors (PRRs) (reviewed by Ingle et al. ).
PAMPs, such as flagellin, lipopolysaccharides, and chitin, are
essential components of many microbes, including human and
plant pathogens, regardless of their location. Detection of PAMPs
by PRRs leads to the activation of a series of defensive responses
that inhibit microbial multiplication and growth. These responses
include production of reactive oxygen species (ROS), alkalini-
zation of the spaces between plant cells, and cell wall reinforce-
ment through deposition of callose and lignin (reviewed by
Gimenez-Ibanez et al. ). Collectively, these responses are
called PAMP-triggered immunity (PTI) (39). Successful plant
pathogens have evolved the capacity to actively suppress PTI by
translocating proteins called effectors into the plant cell using a
TTSS (reviewed by Chisholm et al. ). As plants and patho-
gens co-evolved, plants developed the capacity to detect the
pathogen-produced effectors and to activate stronger and faster
defense responses. This process, called effector triggered im-
munity (ETI), is activated by plant resistance (R) proteins that
‘recognize’ and inhibit the activity of the effector proteins and,
through activation of ETI, suppress microbial multiplication and
spread. Fascinating recent studies suggest that human entero-
bacteria, such as S. enterica serovar Typhimurium, also have the
capacity to actively suppress the plant PTI (74,75). A TTSS
mutant of Salmonella spp. was unable to suppress plant defense
responses, suggesting that Salmonella spp. depend upon the TTSS
during plant infection (65). Furthermore, Salmonella Typhimurium
effectors, introduced into tobacco and Arabidopsis cells via
Agrobacterium tumefaciens transformation or via the TTSS of the
plant pathogen Xanthomonas campestris pv. vesicatoria trans-
Vol. 103, No. 4, 2013 311
formed with the Salmonella Typhimurium effector genes, were
able to suppress PTI responses (74,75). These and other studies
provide strong evidence that human pathogenic microbes com-
municate intimately with plant cells through the delivery of TTSS
effectors, and that these effectors elicit and control plant re-
It is important to remember that since human pathogens cause
human illness merely by being physically present (and viable) in
low numbers, a traditional definition of plant resistance to plant
pathogens may not work as a functionally useful definition of
plant resistance to human pathogens. Yet, if human pathogenic
microbes do produce PAMPs and are able to control plant
responses through injection of TTSS effectors, the implications
would be profound. If plants have evolved resistance mechanisms
that protect against HPOPs as well as plant pathogens, those
pathways can be exploited to minimize HPOP establishment and
colonization on and in plants. In fact, plant hosts that differ-
entially respond to human pathogens already have been identified
(6,8,46,59,65). Different tomato cultivars vary in their abilities to
support colonization by S. enterica, and these differences seem to
be correlated with variation in the types of leaf trichomes present
(6). E. coli O157:H7 colonization patterns on different spinach
cultivars correlated with leaf surface topography (59). Knowing
that plant host variation is associated with resistance or differ-
ences in ability to support human pathogen populations is the first
step in identifying the correlated heritable traits, and integrating
these into crop improvement strategies to reduce the risk of food
Hypothesis: A multihost cycle? The observation that some
enteric bacteria are surprisingly well adapted to persistence on
and in plants raises the question of whether these bacteria, and
perhaps some viruses and parasites as well, that typically are
assigned to a reservoir in the vertebrate gut, could persist in plants
through plant life cycle stages and be present in leaves, fruits or
seeds. Doing so may be an advantage to enteric bacteria whose
vertebrate hosts are herbivores. Presence in the plants that the
herbivores eat may represent a pathway to the next herbivore (Fig.
3). Enteric pathogens will be excreted from the herbivores’ guts
along with undigested seeds of the plants that the herbivore ate,
seeds that will subsequently sprout and produce another genera-
tion of food plants. If the pathogens are either already within or
attached to the seeds, enter the young plant and persist as the
plant grows, then they again have the opportunity to be eaten by a
passing herbivore. Transfer events from herbivore to plant and
from plant to herbivore may be very frequent in the prairie or
pasture. The omnivorous human may encounter the bacteria on
either side of this more complex cycle, by eating either the herbi-
vore or the plants bearing the pathogen. This scenario supports a
previously proposed viewpoint that efforts to reduce the contami-
nation of our food supply should be designed within a holistic
framework, that includes the water, soil, and environments in
which our food plants grow as well as to the more traditional
concerns about safer water, fodder, and environments for our food
Research priorities. Over the past decade we have learned
much about the commonalities among and differences between
HPOPs and plant pathogens, and this growing area of study
informs a larger body of knowledge about foodborne pathogens
and their management. Nonetheless, outbreaks have continued to
occur, and we need to learn much more about the processes by
which foodborne illness arises from the consumption of plant-
based products. The continued challenge of outbreaks associated
with fruits and vegetables led, in 1998, to the provision by the
FDA of general industry guidance for minimizing food safety
hazards (31), and in late 2010 the U.S. Congress passed the FDA
Food Safety Modernization Act (Public Law 111-353), commonly
referred to as FSMA. FSMA calls for a variety of science-based
performance standards focused on major food contaminants.
Significantly, FSMA expands the FDA’s regulatory authority to
the farm level and requires the FDA to establish new, science-
based minimum performance standards for the production and
harvesting of fruit and vegetables (Public Law 111-353; 21
United States Code 350h) (25). This proposed regulation, which
was announced by the FDA on 4 January 2013, addresses water
quality, wildlife incursion, worker sanitation, and other likely
sources of contamination of fresh produce based on available
scientific data (FDA, Docket No. FDA-2011-N-0921). As this
regulation is put into final form and implemented, additional
applied research questions are likely to arise.
To minimize foodborne illnesses associated with HPOPs and, at
the same time, provide scientific information for improving on-
farm production and harvesting standards, we will need to con-
tinue to support targeted rigorous research. It is important to
gather more fundamental knowledge of the biology and genetic
variability of HPOPs, over time and by commodity and location,
the differences in farming practices and other governmental re-
quirements (e.g., conservation or environmental requirements),
and, most importantly, the interactions between the human patho-
gens, plant associated microbes, the host plant, and the environ-
ment. This is not a single simple system; there are issues specific
to each fruit or vegetable cultivar, the location in which it is
grown, and the practices associated with that location. Though
An emerging concept of the ecological
cycle of human enteric pathogens on
humans, animals, and plants. Plant exposure
to human pathogens on plants (HPOP
species) via direct contact with contaminated
manure or indirect contact via bacteria-
carrying water, soil, or other agricultural
elements. Consumption of contaminated or
infected plants by herbivores followed by
shedding of the pathogen in feces,
sometimes along with viable seeds. Humans
can become infected by consumption of
contaminated foods of either kingdom: fresh
fruits and vegetables or meats and dairy
products. Diagram by Angela Records.
most of the work to date has focused on bacterial pathogens, viral,
protozoal and fungal pathogens also must be addressed. It will be
helpful to apply a systems approach that recognizes and takes
advantage of the full cycle. Addressing HPOPs from a disease
cycle perspective brings a number of research questions to mind
(Research Priority Boxes 1 to 5), including aspects of epidemi-
ology, biology, control, surveillance, and ecology.
Next steps: Encouraging multidisciplinary research, exten-
sion, and education through an HPOP Research Coordination
Network. Several years ago, The American Phytopathology
Society’s (APS) Public Policy Board (PPB) began to encourage
more plant pathologists to become involved in efforts to reduce
the risks of HPOPs and to explore opportunities to bring relevant
disciplinary communities together. Plant pathology careers vary
widely and include both fundamental and applied researchers,
educators, and extension agents who work directly with growers
and farmers. While a number of APS members already were
engaged in advancing the science of HPOPs, it was clear that
more could be done. Even plant pathologists who do not work
with HPOPs may have unique, important perspectives that may be
relevant as practical solutions are sought. Furthermore, plant
pathologists will benefit from gaining an appreciation of ap-
proaches typically taken by food microbiologists and epidemiolo-
gists. Leaders from the APS PPB held workshops at the FDA and
the U.S. Department of Agriculture that presented the basics of
plant pathology from the disease cycle to extension. Encouraged
to disseminate our message more broadly to the food safety
community, we held highly successful symposia at the annual
meetings of both the International Association for Food Protec-
tion and APS, both of which brought in food microbiologists and
epidemiologists. Enthusiastic audience participation at those
workshops led to the establishment of the cross-disciplinary APS
Food Safety Interest Group.
Most recently, to further enhance the relationship between our
diverse professions, a multidisciplinary team with broad repre-
sentation from both the plant pathology and food safety com-
munities hosted a research workshop in College Park, MD, in
February 2012 for active researchers and extension pathologists
working on HPOPs. Goals of the meeting were to bring members
of the disciplines together, exchange research strategies and
findings, set research priorities for interdisciplinary coopera-
tion, and develop a mechanism for continuing those interac-
tions into the future. The event, which was funded by a confer-
ence grant from the U.S. Department of Agriculture AFRI Food
Safety Program, attracted over 125 attendees. One highlight was
the announcement by Editor-in-Chief George Sundin of the first-
ever Phytopathology focus issue, to highlight the expanding field
of HPOP research.
To sustain the momentum and further encourage the food safety
and plant pathology communities to work together to reduce the
threat of HPOPs, we propose the establishment of a research
coordination network (RCN). While funding for developing a
network may come from a variety of sources, the U.S. National
Science Foundation (NSF) has supported several RCNs in the
biological and engineering sciences in the past, including the APS
supported RCN for U.S. culture collections. According to the
NSF (www.nsf.gov), RCNs should advance a field or create new
Research Priorities: 2. On the farm
• How can we best communicate risk that may be low, but not
• What can growers do to reduce risk?
• Are there farming practices that may influence the environ-
ment and make it easier or harder for HPOPs to persist?
• How can we develop standards that recognize the dif-
ferences in practices, location, commodities, scope, and miti-
• How do we engage and learn from extension pathologists
and crop consultants?
• How can we best communicate risk that may be low, but not
Research Priorities: 1. The disease cycle
• How often are HPOPs found on or in plants at point
of harvest, or in seeds destined for production of edible
• What are the most important pathways for HPOP contami-
nation of plants? Are there as yet unrecognized vectors and
• What mechanisms do HPOPs use to colonize, persist, and
thrive on plants?
• Are HPOP genes expressed differentially in different hosts/
• Are there elements in the phyllosphere or rhizosphere that
encourage or discourage HPOPs?
• How do human pathogens interact with plant pathogens on
Research Priorities: 4. Basic questions
• Are (some) HPOPs pathogenic to plants?
• Can plant defense responses be harnessed to reduce HPOP
• Do cross kingdom pathogens pose a risk to food safety?
• What additional HPOPs can be identified?
Research Priorities: 5. Other research dilemmas
• How can we establish effective strategies for detecting very
low microbial populations in the field?
• What would an appropriate surrogate model look like?
• How can plant pathology principles be applied to human viruses
(i.e., Norovirus, hepatitis A, etc.) on plants?
Research Priorities: 3. Management strategies
• Are some plant cultivars more resistant to HPOPs than others?
• What active resistance mechanisms and natural inhibitors do
plants use against HPOPs?
• Can we make plants more resistant to colonization by HPOPs?
• Can epiphytic phylloplane microbes trigger plant resistance to
Vol. 103, No. 4, 2013 313
directions in research and education. A successful NSF RCN
would gain support for fostering collaborations (domestic and
international) and multidisciplinary activities. An HPOP RCN can
provide an opportunity for collaborations between extension
educators and agents, growers, and scientists (plant pathologists,
food microbiologists, and epidemiologists) in academia, govern-
ment, and industry. It can serve to facilitate the development of
multidisciplinary proposals aimed at addressing some of the
fundamental and applied questions. It also may allow us to bring
to the HPOPs field additional plant pathologists with expertise in
understanding plant–microbe interactions and to prepare exten-
sion personnel to assist growers in understanding and compliance
with new production and harvesting standards. Finally, an HPOP
RCN will allow us to continue to expand our understanding of the
entire HPOPs system—the full disease cycle.
We thank A. Records for contributing the original artwork in Figure 3
and for adapting material from Ritchie (68) for Figure 2.
1. Abramovitch, R. B., Anderson, J. C., and Martin, G. B. 2006. Bacterial
elicitation and evasion of plant innate immunity. Nat. Rev. Mol. Cell.
2. Aruscavage, D., Phelan, P. L., Lee, K., and LeJeune, J. T. 2010. Impact of
changes in sugar exudate created by biological damage to tomato plants
on the persistence of Escherichia coli O157:H7. J. Food Sci. 75:187-192.
3. Barak, J. 2004. Biofilms and other strategies exploited by salmonella and
friends on plants. (Abstr.) Phytopathology 94(suppl.):S128.
4. Barak, J. D., Gorski, L., Naraghi-Arani, P., and Charkowski, A. O. 2005.
Salmonella enterica virulence genes are required for bacterial attachment
to plant tissue. Appl. Environ. Microbiol. 71(10):5685-5691. doi:10.1128/
5. Barak, J. D., Jahn, C. E., Gibson, D. L., and Charkowski, A. O. 2007. The
role of cellulose and O-antigen capsule in the colonization of plants by
Salmonella enterica. Mol. Plant-Microbe Interact. 20:1083-1091. doi:
6. Barak, J. D., Kramer, L. C., and Hao, L. Y. 2011. Colonization of tomato
plants by Salmonella enterica is cultivar dependent, and type 1 trichomes
are preferred colonization sites. Appl. Environ. Microbiol. 77(2):498-504.
7. Barak, J. D., and Liang, A. S. 2008. Role of soil, crop debris, and a plant
pathogen in Salmonella enterica contamination of tomato plants. PLoS
One 3(2). doi:10.1371/Journal.Pone.0001657
8. Barak, J. D., Liang, A., and Narm, K. E. 2008. Differential attachment to
and subsequent contamination of agricultural crops by Salmonella
enterica. Appl. Environ. Microbiol. 74(17):5568-5570. doi:10.1128/
9. Barak, J. D., and Schroeder, B. K. 2012. Interrelationships of food safety
and plant pathology: The life cycle of human pathogens on plants. Annu.
Rev. Phytopathol. 50:241-266. doi:10.1146/annurev-phyto-081211-172936
10. Barton Behravesh, C., Mody, R. K., Jungk, J., Gaul, L., Redd, J. T., Chen,
S., Cosgrove, S., Hedican, E., Sweat, D., Chavez-Hauser, L., Snow, S. L.,
Hanson, H., Nguyen, T. A., Sodha, S. V., Boore, A. L., Russo, E.,
Mikoleit, M., Theobald, L., Gerner-Smidt, P., Hoekstra, R. M., Angulo,
F. J., Swerdlow, D. L., Tauxe, R. V., Griffin, P. M., Williams, I. T., and
Salmonella Saintpaul Outbreak Investigation, T. 2011. 2008 outbreak of
Salmonella Saintpaul infections associated with raw produce. N. Engl. J.
Med. 364(10):918-927. doi:10.1056/NEJMoa1005741
11. Barton-Behravesh, C., Williams, I. T., and Tauxe, R. V. 2012. Emerging
foodborne pathogens and problems: Expanding prevention efforts before
slaughter or harvest. Pages 307-331 in: Improving Food Safety Through a
One Health Approach; Workshop Summary. E. Choffnes, D. Relman, L.
Olsen, R. Hutton, and A. Mack, eds. The National Academies Press,
12. Berger, C. N., Sodha, S. V., Shaw, R. K., Griffin, P. M., Pink, D., Hand, P.,
and Frankel, G. 2010. Fresh fruit and vegetables as vehicles for the
transmission of human pathogens. Environ. Microbiol. 12(9):2385-2397.
13. Beuchat, L. 1998. Surface decontamination of fruits and vegetables eaten
raw: A review. http://www.who.int/foodsafety/publications/fs_management/
surfac_decon/en/. Accessed Oct 20, 2003. World Health Organization,
Food Saftety Unit, Geneva.
14. Bowen, A., Fry, A., Richards, G., and Beuchat, L. 2006. Infections
associated with cantaloupe consumption: A public health concern.
Epidemiol. Infect. 134(4):675-685. doi:10.1017/S0950268805005480
15. Brandl, M. T. 2006. Fitness of human enteric pathogens on plants and
implications for food safety. Annu. Rev. Phytopathol. 44:367-392. doi:
16. Brandl, M. T. 2008. Plant lesions promote the rapid multipication of
Escherichia coli O157:H7 on postharvest lettuce. Appl. Environ. Micro-
17. CDC. 2011. Multistate outbreak of Listeriosis linked to whole cantaloupes
from Jensen Farms, Colorado. http://www.cdc.gov/listeria/outbreaks/
18. Chisholm, S. T., Coaker, G., Day, B., and Staskawicz, B. J. 2006. Host-
microbe interactions: Shaping the evolution of the plant immune
response. Cell 124:803-914.
19. Crepin, A., Beury-Cirou, A., Barbey, C., Farmer, C., Helias, V., Burini, J.
F., Faure, D., and Latour, X. 2012. N-Acyl Homoserine lactones in diverse
Pectobacterium and Dickeya plant pathogens: Diversity, abundance, and
involvement in virulence. Sensors 12:3484-3497.
20. Danhorn, T., and Fuqua, C. 2007. Biofilm formation by plant-associated
bacteria. Annu. Rev. Microbiol. 61:401-422. doi:10.1146/annurev.micro.
21. Deering, A. J., Mauer, L. J., and Pruitt, R. E. 2012. Internalization of E.
coli O157:H7 and Salmonella spp. in plants: A review. Food Res. Int.
22. Dong, Y. H., Wang, L. H., Xu, J. L., Zhang, H. B., Zhang, X. F., and
Zhang, L. H. 2001. Quenching quorum-sensing-dependent bacterial
infection by an N-acyl homoserine lactonase. Nature 411(6839):813-817.
23. Doyle, M. P., and Erickson, M. C. 2012. Opportunities for mitigating
pathogen contamination during on-farm food production. Int. J. Food
24. Erickson, M. 2012. Internalization of fresh produce by foodborne
pathogens. Annu. Rev. Food Sci.Technol. 3:283-310.
25. FDA. 2013. Standards for growing, harvesting, packing and holding of
produce for human consumption. http://www.ofr.gov/OFRUpload/
26. Fett, W. F. 2000. Naturally occurring biofilms on alfalfa and other types
of sprouts. J. Food Prot. 63:625-632.
27. Fett, W. F., and Cooke, P. H. 2005. Native microbial aggregates on alfalfa,
clover and mung bean sprout cotyledons for thickness as determined by
confocal scanning laser microscopy. Food Microbiol. 22:253-259.
28. Gautam, D., Payton, M., Fletcher, J., and Ma, L. 2012. Surface survival
and internalization of Salmonella through natural cracks on developing
cantaloupe fruit, alone or in the presence of the plant pathogen Erwinia
tracheiphila. International Association of Food Protection Annual
Meeting, Providence, RI.
29. Gimenez-Ibanez, S., and Rathjen, J. P. 2010. The case for the defense:
Plants versus Pseudomonas syringae. Microbes Infect. 12:428-437.
30. Gu, G. Y., Hu, J. H., Cevallos-Cevallos, J. M., Richardson, S. M., Bartz, J.
A., and van Bruggen, A. H. C. 2011. Internal colonization of Salmonella
enterica serovar Typhimurium in tomato plants. Plos One 6(11).
31. Guidance for Industry: Guide to Minimize Microbial Food Safety
Hazards for Fresh Fruits and Vegetables. 1998. FDA Center for Food
Safety and Applied Nutrition, Washington, DC. http://www.fda.gov/Food/
32. Guo, X. 2001. Survival of Salmonellae on and in tomato plants from the
time of inoculation at flowering and early stages of fruit development
through fruit ripening. Appl. Environ. Microbiol. 67:4760-4764.
33. Gupta, S. K., Nalluswami, K., Snider, C., Perch, M., Balasegaram, M.,
Burmeister, D., Lockett, J., Sandt, C., Hoekstra, R. M., and Montgomery,
S. 2007. Outbreak of Salmonella Braenderup infections associated with
Roma tomatoes, northeastern United States, 2004: A useful method for
subtyping exposures in field investigations. Epidemiol. Infect. 135(7):
34. Hancock, D., Besser, T., and Rice, D. 1998. Ecology of Escherichia coli
O157:H7 in cattle and impact of management practices. Pages 85-91 in:
Escherichia coli O157:H7 and Other Shiga Toxin-Producing E. coli
Strains. J. Kaper and A. O’Brien, eds. ASM Press, Washington, DC.
35. Hao, L. Y., Willis, D. K., Andrews-Polymenis, H., McClelland, M., and
Barak, J. D. 2012. Requirement of siderophore biosynthesis for plant
colonization by Salmonella enterica. Appl. Environ. Microbiol. 78(13):
36. He, J., Baldini, R. L., Déziel, E., Saucier, M., Zhang, Q., Liberati, N. T.,
Lee, D., Urbach, J., Goodman, H. M., and Rahme, L. G. 2004. The broad
host range pathogen Pseudomonas aeruginosa strain PA14 carries two
pathogenicity islands harboring plant and animal virulence genes. Proc.
Natl. Acad. Sci. U.S.A. 101(8):2530-2535. doi:10.1073/pnas.0304622101
37. Heuer, H., Schmitt, H., and Smalla, K. 2011. Antibiotic resistance gene
spread due to manure application on agricultural fields. Curr. Opin.
Microbiol. 14(3):236-243. doi:10.1016/j.mib.2011.04.009
38. Hilborn, E. D., Mermin, J. H., Mshar, P. A., Hadler, J. L., Voetsch, A.,
Wojtkunski, C., Swartz, M., Mshar, R., Lambert-Fair, M. A., Farrar, J. A.,
Glynn, M. K., and Slutsker, L. 1999. A multistate outbreak of Escherichia
coli O157:H7 infections associated with consumption of mesclun lettuce.
Arch. Intern. Med. 159(15):1758-1764.
39. Ingle, R. A., Carstens, M., and Denby, K. J. 2006. PAMP recognition and
the plant-pathogen arms race. BioEssays 28:880-889.
40. Iniguez, A. L., Dong, Y. M., Carter, H. D., Ahmer, B. M. M., Stone, J. M.,
and Triplett, E. W. 2005. Regulation of enteric endophytic bacterial
colonization by plant defenses. Mol. Plant-Microbe Interact. 18:169-178.
41. Islam, M., Doyle, M. P., Phatak, S. C., Millner, P., and Jiang, X. P. 2004.
Persistence of enterohemorrhagic Escherichia coli O157:H7 in soil and
on leaf lettuce and parsley grown in fields treated with contaminated
manure composts or irrigation water. J. Food Prot. 67(7):1365-1370.
42. Islam, M., Morgan, J., Doyle, M. P., Phatak, S. C., Millner, P., and Jiang,
X. P. 2004. Fate of Salmonella enterica serovar Typhimurium on carrots
and radishes grown in fields treated with contaminated manure composts
or irrigation water. Appl. Environ. Microbiol. 70(4):2497-2502. doi:
43. Itoh, Y., Sugita-Konishi, Y., Kasuga, F., Iwaki, M., Hara-Kudo, Y., Saito,
N., Noguchi, Y., Konuma, H., and Kumagai, S. 1998. Enterohemorrhagic
Escherichia coli O157:H7 present in radish sprouts. Appl. Environ.
44. Jaquette, C. B., Beuchat, L. R., and Mahon, B. E. 1996. Efficacy of
chlorine and heat treatment in killing Salmonella stanley inoculated onto
alfalfa seeds and growth and survival of the pathogen during sprouting
and storage. Appl. Environ. Microbiol. 62(7):2212-2215.
45. Kisluk, G., and Yaron, S. 2012. Presence and persistence of Salmonella
enterica serotype Typhimurium in the phyllosphere and rhizosphere of
spray-irrigated parsley. Appl. Environ. Microbiol. 78(11):4030-4036.
46. Klerks, M. M., Franz, E., van Gent-Pelzer, M., Zijlstra, C., and van
Bruggen, A. H. C. 2007. Differential interaction of Salmonella enterica
serovars with lettuce cultivars and plant-microbe factors influencing the
colonization efficiency. ISME J. 1(7):620-631. doi:10.1038/ismej.2007.82
47. Kroupitski, Y., Golberg, D., Belausov, E., Pinto, R., Swartzberg, D.,
Granot, D., and Sela, S. 2009. Internalization of Salmonella enterica in
leaves is induced by light and involves chemotaxis and penetration
through open stomata. Appl. Environ. Microbiol. 75(19):6076-6086.
48. Kroupitski, Y., Pinto, R., Brandl, M. T., Belausov, E., and Sela, S. 2009.
Interactions of Salmonella enterica with lettuce leaves. J. Appl.
Microbiol. 106(6):1876-1885. doi:10.1111/j.1365-2672.2009.04152.x
49. Lapidot, A., Romling, U., and Yaron, S. 2006. Biofilm formation and the
survival of Salmonella Typhimurium on parsley. Int. J. Food Microbiol.
50. Lapidot, A., and Yaron, S. 2009. Transfer of Salmonella enterica serovar
Typhimurium from contaminated irrigation water to parsley is dependent
on curli and cellulose, the biofilm matrix components. J. Food Prot.
51. Lindow, S. E., and Brandl, M. T. 2003. Microbiology of the phyllosphere.
Appl. Environ. Microbiol. 69(4):1875-1883.
52. Lugtenberg, B. J., Chin, A. W. T. F., and Bloemberg, G. V. 2002.
Microbe–plant interactions: Principles and mechanisms. Antonie Van
53. Lynch, M. F., and Tauxe, R. V. 2009. Salmonellosis: Nontyphoidal.
Chapter 32 in: Bacterial Infections of Humans, 4th ed. P. S. Brachman
and E. Abrutyn, eds. Springer, New York.
54. Lynch, M. F., Tauxe, R. V., and Hedberg, C. W. 2009. The growing
burden of foodborne outbreaks due to contaminated fresh produce:
Risks and opportunities. Epidemiol. Infect. 137(3):307-315. doi:10.1017/
55. Macovei, L., Miles, B., and Zurek, L. 2008. The potential of house flies to
contaminate ready-to-eat food with antibiotic resistant enterococci. J.
Food Prot. 71:432-439.
56. McManus, P. S., Stockwell, V. O., Sundin, G. W., and Jones, A. L. 2002.
Antibiotic use in plant agriculture. Annu. Rev. Phytopathol. 40:443-465.
57. Melotto, M., Underwood, W., and He, S. Y. 2008. Role of stomata in plant
innate immunity and foliar bacterial diseases. Annu. Rev. Phytopathol.
58. Melotto, M., Underwood, W., Nomura, K., and He, S. Y. 2006. Plant
stomata function in innate immunity against bacterial infection. Cell 126:
59. Mitra, R., Cuesta-Alonso, E., Wayadande, A., Talley, J., Gilliland, S., and
Fletcher, J. 2009. Effect of route of introduction and host cultivar on the
colonization, internalization, and movement of the human pathogen
Escherichia coli O157:H7 in spinach. J. Food Prot. 72:1521-1530.
60. Mody, R. K., Greene, S. A., Gaul, L., Sever, A., Pichette, S., Zambrana, I.,
Dang, T., Gass, A., Wood, R., Herman, K., Cantwell, L. B., Falkenhorst,
G., Wannemuehler, K., Hoekstra, R. M., McCullum, I., Cone, A.,
Franklin, L., Austin, J., Delea, K., Behravesh, C. B., Sodha, S. V., Yee, J.
C., Emanuel, B., Al-Khaldi, S. F., Jefferson, V., Williams, I. T., Griffin, P.
M., and Swerdlow, D. L. 2011. National outbreak of Salmonella serotype
saintpaul infections: Importance of Texas restaurant investigations in
implicating jalapeno peppers. PLoS One 6(2):e16579. doi:10.1371/
61. Morris, C. E., and Monier, J. M. 2003. The ecological significance of
biofilm formation by plant-associated bacteria. Annu. Rev. Phytopathol.
62. Olaimat, A. N., and Holley, R. A. 2012. Factors influencing the microbial
safety of fresh produce: A review. Food Microbiol. 32(1):1-19.
63. Osterholm, M. T., Ostrowsky, J., Farrar, J. A., Gravani, R. B., Tauxe, R.
V., Buchanan, R. L., and Hedberg, C. W. 2009. A novel approach to
enhance food safety: Industry-academia-government partnership for
applied research. J. Food Prot. 72:1509-1512.
64. Penteado, A. L., Eblen, B. S., and Miller, A. J. 2004. Evidence of
Salmonella internalization into fresh mangos during simulated postharvest
insect disinfestation procedures. J. Food Prot. 67:181-184.
65. Quilliam, R. S., Williams, A. P., and Jones, D. L. 2012. Lettuce cultivar
mediates both phyllosphere and rhizosphere activity of Escherichia coli
O157:H7. Plos One 7(3). doi:10.1371/journal.pone.0033842
66. Raymundo, A. K., and Ries, S. M. 1980. Chemotaxis of Erwinia amylo-
vora. Phytopathology 70:1066-1069.
67. Riedel, K., Hentzer, M., Geisenberger, O., Huber, B., Steidle, A., Wu, H.,
Hoiby, N., Givskov, M., Molin, S., and Eberl, L. 2001. N-Acylhomo-
serine-lactone-mediated communication between Pseudomonas aerugi-
nosa and Burkholderia cepacia in mixed biofilms. Microbiology
68. Ritchie, D. F. 2000. Bacterial spot of pepper and tomato. The Plant Health
69. Roper, M. C. 2011. Pantoea stewartii subsp. stewartii: Lessons learned
from a xylem-dwelling pathogen of sweet corn. Mol. Plant Pathol.
70. Rosenblueth, M., and Martinez-Romero, E. 2006. Bacterial endophytes
and their interactions with hosts. Mol. Plant-Microbe Interact. 19:827-
71. Rushing, J. W., Angulo, F. J., Beuchat, L. R. 1996. Implementation of a
HACCP program in a commercial fresh-market tomato packinghouse: A
model for the industry. Dairy Food Environ. Sanit. 16:549-553.
72. Saldaña, Z., Sánchez, E., Xicohtencatl-Cortes, J., Puente, J. L., and Giron,
J. A. 2011. Surface structures involved in plant stomata and leaf
colonization by Shiga-toxigenic Escherichia coli O157:H7. Front.
73. Schikora, A., Garcia, A. V., and Hirt, H. 2012. Plants as alternative hosts
for Salmonella. Trends Plant Sci. 17(5):245-249. doi:10.1016/j.tplants.
74. Schikora, A., Virlogeux-Payant, I., Bueso, E., Garcia, A. V., Nilau, T.,
Charrier, A., Pelletier, S., Menanteau, P., Baccarini, M., Velge, P., and
Hirt, H. 2011. Conservation of Salmonella infection mechanisms in plants
and animals. Plos One 6(9). doi:10.1371/journal.pone.0024112
75. Shirron, N., and Yaron, S. 2011. Active suppression of early immune
response in tobacco by the human pathogen Salmonella Typhimurium.
PLoS One 6(4):e18855. doi:10.1371/journal.pone.0018855
76. Silo-Suh, L., Suh, S.-J., Sokol, P. A., and Ohman, D. E. 2002. A simple
alfalfa seedling infection model for Pseudomonas aeruginosa strains
associated with cystic fibrosis shows AlgT (sigma-22) and RhlR
contribute to pathogenesis. Proc. Natl. Acad. Sci. U.S.A. 99(24):15699-
77. Sivapalasingam, S., Friedman, C. R., Cohen, L., and Tauxe, R. V. 2004.
Fresh produce: a growing cause of outbreaks of foodborne illness in the
United States, 1973 through 1997. J. Food Prot. 67(10):2342-2353.
78. Smith, J. L., Fratamico, P. M., and Yan, X. 2011. Eavesdropping by
bacteria: The role of SdiA in Escherichia coli and Salmonella enterica
serovar Typhimurium quorum sensing. Foodborne Pathog. Dis. 8(2):169-
79. Staskawicz, B. J., Mudgett, M. B., Dangl, J. L., and Galan, J. E. 2001.
Common and contrasting themes of plant and animal diseases. Science
80. Talley, J. L., Wayadande, A. C., Wasala, L. P., Gerry, A. C., Fletcher, J.,
DeSilva, U., and Gilliland, S. E. 2009. Association of Escherichia coli
O157:H7 with filth flies (Muscidae and Calliphoridae) captured in leafy
greens fields and experimental transmission of E. coli O157:H7 to spinach
Vol. 103, No. 4, 2013 315 Download full-text
leaves by house flies (Diptera: Muscidae). J. Food Prot. 72:1547-1552.
81. Telford, J. L., Barocchi, M. A., Margarit, I., Rappuoli, R., and Grandi, G.
2006. Gram positive pathogens. Nat. Rev. Microbiol. 4:509-519.
82. Teplitski, M., Barak, J. D., and Schneider, K. R. 2009. Human enteric
pathogens in produce: Un-answered ecological questions with direct
implications for food safety. Curr. Opin. Plant Biotechnol. 20:166-171.
83. Teplitski, M., Noel, J. T., Alagely, A., and Danyluk, M. D. 2012.
Functional genomics studies shed light on the nutrition and gene ex-
pression of non-typhoidal Salmonella and enterovirulent E. coli in pro-
duce. Food Res. Int. 45(2):576-586. doi:10.1016/j.foodres.2011.06.020
84. Vidaver, A. K., Tolin, S., and Lambrecht, P. 2006. Laboratory, growth
chamber and greenhouse microbial safety: Plant pathogens and plant
associated microorganisms of significance to human health. In: Biological
Safety: Principles and Practices. D. O. Fleming and D. L. Hunt, eds. ASM
Press, Washington, DC.
85. Wagenaar, J. 2008. Poultry colonization with Campylobacter and its
control at the primary production level. Chapter 37 in: Campylobacter.
C. S. I. N. Nachamkin, C. M. Scymanski, and M. Blaser, eds. ASM Press,
86. Wells, J. M., and Butterfield, J. E. 1997. Salmonella contamination
associated with bacterial soft rot of fresh fruits and vegetables in the
marketplace. Plant Dis. 81:867-872.
87. Wendel, A. M., Johnson, D. H., Sharapov, U., Grant, J., Archer, J. R.,
Monson, T., Koschmann, C., and Davis, J. P. 2009. Multistate outbreak of
Escherichia coli O157:H7 infection associated with consumption of
packaged spinach, August-September 2006: The Wisconsin investigation.
Clin. Infect. Dis. 48(8):1079-1086. doi:10.1086/597399
88. Wheeler, C., Vogt, T. M., Armstrong, G. L., Vaughan, G., Weltman, A.,
Nainan, O. V., Dato, V., Xia, G., Waller, K., Amon, J., Lee, T. M.,
Highbaugh-Battle, A., Hembree, C., Evenson, S., Ruta, M. A., Williams,
I. T., Fiore, A. E., and Bell, B. P. 2005. An outbreak of hepatitis A associ-
ated with green onions. New Engl. J. Med. 353:890-897. doi:10.1056/
89. Winfield, M. D., and Groisman, E. A. 2003. Role of nonhost
environments in the lifestyles of Salmonella and Escherichia coli. Appl.
Environ. Microbiol. 69(7):3687-3694.
90. You, Y., Rankin, S. C., Aceto, H. W., Benson, C. E., Toth, J. D., and Dou,
Z. 2006. Survival of Salmonella enterica serovar Newport in manure and
manure-amended soils. Appl. Environ. Microbiol. 72(9):5777-5783.
91. Zeng, W., Melotto, M., and He, S. Y. 2010. Plant stomata: A checkpoint of
host immunity and pathogen virulence. Curr. Opin. Biotechnol. 21:599-