Immunity in Plants and Animal

8/14/2019 Immunity in Plants and Animal

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Review of innate and specific immunity in plants and

animalsMarcello Iriti Franco Faoro

Received: 19 March 2007 / Accepted: 9 May 2007 / Published online: 7 June 2007

Springer Science+Business Media B.V. 2007

Abstract Innate immunity represents a trait com-

mon to plants and animals, based on the recognition

of pathogen associated molecular patterns (PAMPs)

by the host pattern recognition receptors (PRRs). It is

generally assumed that a pathogen strain, or race,

may have elaborated mechanisms to suppress, or

evade, the PAMP-triggered immunity. Once this plan

was successful, the colonization would have been

counteracted by an adaptive strategy that a plant

cultivar must have evolved as a second line of

defence. In this co-evolutionary context, adaptiveimmunity and host resistance (cultivar-pathogen race/

strain-specific) has been differently selected, in

animals and plants respectively, to face specialized

pathogens. Notwithstanding, plant host resistance,

based on matching between resistance (R) and

avirulence (avr) genes, represents a form of innate

immunity, being R proteins similar to PRRs, although

able to recognize specific virulence factors (avr

proteins) rather than PAMPs. Besides, despite the

lack of adaptive immunity preserved plants from

autoimmune disorders, inappropriate plant immuneresponses may occur, producing some side-effects, in

terms of fitness costs of induced resistance and

autotoxicity. A set of similar defence responses

shared from plants and animals, such as defensins,

reactive oxygen species (ROS), oxylipins and pro-

grammed cell death (PCD) are briefly described.

Keywords Adaptive immunity Autoimmunity

Autotoxicity Fitness costs innate immunity SAR

Introduction

Either plants and animals are capable of recognizing

and distinguishing between self and non-self. How-

ever, some phylogenetically ancient structures and

strategies used in defence have been retained by

parallel evolution, while some others appeared more

recently during phylogenesis [1, 2].

In this context, innate immunity, common to plants

and animals, deeply differs from the adaptive one,

which is restricted to vertebrates. Plants, lacking

immunoglobulin molecules, circulating immune cellsand phagocytic processes, do not possess any adap-

tive immunity, despite an array of innate defence

mechanisms. Innate immunity can be considered as a

battery of first-line defences against microbes, that

pre-exists pathogen challenging and adaptive immu-

nity triggering in animals [3].

Recognition of PAMPs (pathogen associated

molecular patterns) represents the major trait of

innate immunity common to plants and animals,

M. Iriti (&) F. Faoro

Plant Pathology Institute, University of Milan,

Via Celoria 2, Milan 20133, Italy

e-mail: [email protected]

M. Iriti F. Faoro

CNR, Plant Virology Institute, U.O. Milan, Italy

123

Mycopathologia (2007) 164:5764

DOI 10.1007/s11046-007-9026-7


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with the paradigm of drosophila toll receptors,

mammalian TLRs (toll-like receptors) and the

products of R (resistance) genes in plants, collec-

tively termed as pattern recognition receptors

(PRRs) [4]. Thus, PAMPs, more commonly known

as general elicitors in plants, including lipopolysac-

charides (LPS), peptidoglycans, flagellin, microbialcell wall fragments, phospholipids, proteins, double

stranded RNA and methylated DNA, are able to

elicit a host defence response by binding to

receptors [5]. Besides, innate immunity receptors,

both in plants and animals, are nonclonal and

encoded in the germline, unlike B and T lymphocyte

receptors, which are otherwise clonal and rearranged

during development following somatic recombina-

tions, in addition to be responsible for immunologic

memory [6].

Perhaps, in this scenario, plants avoid the mainharmful side effect of adaptive immunity, that is

autoimmunity, due to abnormalities in self tolerance

and the subsequent immune response to self antigens,

though plant fitness costs, particularly in conditions

of low pathogen pressure, might be somewhat

identified with a sort of autoimmune disease [7].

The host-pathogen interaction

In animals, fungi causing mycoses consist of twoclasses. The primary pathogens infect healthy non-

compromised individuals, whereas the opportunistic

fungi cause disease in immunodeficient patients, as

those receiving immunosuppressive therapy, under-

going bone marrow or solid organ transplantation or

with acquired immunodeficiency syndrome (AIDS)

[8, 9]. In plants, fungal pathogens can be divided into

obligate and nonobligate parasites. The former, also

known as biotrophs, can growth, develop and mul-

tiply only in close association with their living host,

during their entire life cycle, while the latter can live

on either living and dead hosts and nutrient media,

requiring the plant only for a part of their life cycle.

In addition, nonobligate parasites include facultative

saprophytes or facultative parasites (or necrotrophs),

depending on their main habitus, parasitic or sapro-

phytic respectively [10].With regard to infection process, two different

routes exist in animals. The endogenous infection

route pertains to the commensal body flora, depend-

ing on overgrowth of fungal strains (i.e. Candida

albicans, Fig. 1a), at the nonsterile sites where they

perform their commensalisms, such as stomatogna-

thic system, digestive and respiratory tract and genital

organs, or following translocation from these sites

towards body compartments that react to their

presence. Differently, the exogenous infection route

is due to the entry of saprobes from the environmentto the human body, usually through the airways and

pulmonary tree [8, 11]. Plant pathogenic fungi show a

rather similar behaviour, invading their hosts after

entering through epigeous organs (leaves and stem),

such as rust fungi (Fig. 1b) and downy mildews, or

hypogeous organs (roots), for instance Rhizoctonia

solani [10]. However, a downright endogenous

infection route does not exist, although symbiosis

between plants and fungi frequently occur. Myco-

rryzhae are mutualistic associations taking place at

the root level (rizhosphere), where the fungus profitsby the carbohydrates assimilated from the plant, and

the latter, in return, benefits from the fungal hyphae

to improve its own mineral nutrient uptake by roots.

Interestingly, mycorryzhae may elicit plant defence

mechanisms by releasing chitin or chitosan frag-

ments, sensing as PAMPs from the host perception

machinery [12].

Nevertheless, another evident divergence, between

the animal and plant kingdom, concerns the different

relevance covered by the fungal diseases in animal

Fig. 1 Pathogenic fungi of

animals and plants; (a)

Candida albicans in human

oral mucosa (Periodic Acid-

Shiff staining) and (b)

Uromyces appendiculatus

in bean leaf parenchyma

(Evans blue staining)

58 Mycopathologia (2007) 164:5764

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and plant pathology. In the latter, diseases caused by

fungi include the most diffuse and damaging ones, in

contrast to the minor importance of mycoses among

the infectious diseases.

The host immune response in plants and animals

After pathogen challenging, the immune system

provides protection against the infection spreading.

In plants, innate immunity is the only way to

counteract the disease progression while in verte-

brates adaptive immunity, either humoural or cell-

mediated, is also triggered. Thus plants apparently

lack in a part of their immune system able to adapt

according to the changeable events [1, 6, 13].

At the host-fungus interface, plant/animal surface

barriers firstly oppose to pathogen penetration. Intactcutaneous tissues, mucous membranes and respira-

tory tract lining fluid prevent the infection in animal

world, as well as leaf epicuticular layers, suberized,

cutinized and lignified epidermal tissues do in plants.

Nevertheless all these outermost barriers can be

variously overcome from the pathogenic fungi [14,

15]. If it occurs, pathogen recognition represents the

first step at the onset of the host immune response. In

animals, PRRs are involved in recognition of PAMPs

derived from Candida albicans, Aspergillus fumiga-

tus, Cryptococcus neoformans, Pneumocystis cariniiand Saccharomyces cerevisiae. Particularly, TLR2

and TLR4 recognize constituents of fungal cell wall

and membrane, such as glucans, mannan, proteins,

glycolipids and yeast zymosan [4, 16]. Similarly,

plants recognize glucans, chitin, chitosan, ergosterol,

sphingolipids by means of binding proteins involved

in pathogen perception, signal transduction and

immunity [5]. In this short survey, the attention is

focused on some components of the innate immunity

shared by animal and plant world, precisely defen-

sins, reactive oxygen species (ROS), oxylipins andprogrammed cell death (PCD, Fig. 2).

Defensins

These are basic, small, cysteine-rich peptides (up to

50 amino-acids with at least two excess positive

charges due to lysine and arginine residues) with a

broad-spectrum antibiotic activity. In animals, they

are particularly abundant in granules of leukocytes

and epithelia, where they are either constitutive and

induced by infection [17]. In plants, defensins arefound constitutively in storage organs (seeds) and

peripheral cell layers of generative tissues (reproduc-

tive organs, fruits and flowers), besides being

induced, in vegetative tissues, following infection or

wounding [18]. Generally, the activity of these

cationic antimicrobial peptides is related to their

membranolytic properties. Due to their amphipathic

characteristics, animal defensins target microbial

membranes, inducing ion-permeable pores in lipid

bilayers [17]. Otherwise, plant defensins alter the

structural integrity of fungal membranes by interact-ing specifically with fungal sphingolipids and induc-

ing membrane permeabilization, in turn resulting in

increased calcium influx, potassium efflux and

reduced fungal growth [18].

dicaci)n(elonil dicaci)n(elonil

PMAP PMAP

dicacinodihcarA dicacinodihcarA

SNISNEFED,SOR SNISNEFED,SOR

setanomsaJ/sdionacedatcO setanomsaJ/sdionacedatcO

RRP RRP

DCP DCP

yticixottceriD yticixottceriD

SOA SOA

XOL XOL

COA COA

XOL XOL

seneirtokueL seneirtokueL

XOC XOC

,snidnalgatsorPsenaxobmorhT,snidnalgatsorPsenaxobmorhT

sdionasociE sdionasociE

RRP RRP

PMAP PMAPFig. 2 Defence

mechanisms common to

plants and animals; (AOC,

allene oxide cyclase; AOS,

allene oxide synthase;

COX, cyclooxygenase;LOX, lipoxygenase; PAMP,

pathogen associated

molecular pattern; PCD,

programmed cell death;

PRR, pathogen recognition

receptor; ROS, reactive

oxygen species)

Mycopathologia (2007) 164:5764 59

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ROS

The production of reactive oxygen species (ROS) is

another defence reaction that occurs both in animal

and plant world. In animals, during inflammation and

immune response, the activated phagocytic white

cells (neutrophils, macrophages, monocytes) gener-ate, in their vacuoles, superoxide radical (O2

) by a

NADPH oxidase. This radical species is then trans-

formed in other ROS (mainly hydrogen peroxide,

H2O2, and hydroxyl radical,.OH) involved in direct

toxicity towards microbes, in a process known as

respiratory burst [19]. Similarly, in plant cells,

oxidative burst occurs as an early defence response.

A plasma membrane located NADPH oxidase, shar-

ing homology with its mammalian counterpart,

produces .O2, contributing, in conjunction to other

ROS, to create a hostile apoplastic (extracellular)environment for the pathogen. Interestingly, any plant

cell can mount a defence response, as proved, for

instance, by the presence of a NADPH oxidase in

many cell types and tissues and by the competence to

synthesize phytoalexins. This would compensate for

the absence of a true immune system, meant as cells,

tissues and organs deputed to defence.

Enzymes involved in ROS chemistry are the same

in all pluricellular eucaryotic organisms. The enzyme

superoxide dismutase (SOD) rapidly convert .O2 to

H2O2, which may form OH in presence of transitionmetal ions, according to the HaberWeiss and Fenton

reactions [20]. Nonetheless, the mechanisms involved

in the homeostasis of the cell redox status, including

non-enzymatic and enzymatic scavengers, differ to

some extent between the two kingdoms [21]. Any-

how, the failure of respiratory burst causes chronic

granulomatous disease, in animals, characterized by

life-threatening pyogenic infections and inflamma-

tory granulomas, as well as defective oxidative burst

impairs, in plants, the defence response orchestrated

by ROS [20, 22].

Oxylipins

These are metabolites produced by the oxidation of

polyunsaturated fatty acids (PUFAs), after their

discharge from the lipid bilayers due to phospholip-

ases. Afterwards, free arachidonic and linole(n)ic

acid, the main PUFAs in the biological membranes of

animals and plants respectively, undergo oxidation

via an array of oxygenases, able to catalyze the

incorporation of oxygen atoms into PUFAs. Thus,

lipoxygenases consume a molecule of oxygen to

initiate the synthesis of leukotrienes in animals,

whereas, in plants, the dioxygenation of a-linolenic

acid is followed by other two enzymatic steps,

catalyzed by the Allene Oxide Synthase (AOS) andAllene Oxide Cyclase (AOC), leading to jasmonates

synthesis [23] (Fig. 2). Alternatively, cyclooxygen-

ases (COX) converts arachidonic acid to prostaglan-

dins a nd thromboxane s (c ollec tive ly na me d

prostanoids) consuming two molecules of oxygen,

in animals, whereas a pathogen-induced oxidase

(PIOX), with homology to COX, similarly leads to

another class of lipid mediators in plants. Either

jasmonates, or octadecanoids, and prostanoids and

leukotrienes, collectively named eicosanoids, exhibit

similar functions in plants and animals respectively,particularly as regards defence mechanisms [24].

Octadecanoids are involved both in physiological

processes, such as flowering and fruit ripening, and in

host defence response to pathogens, wounding and

environmental stresses [25]. Likewise, eicosanoids

play a major role in the regulation of vascular tone,

inflammation, infection and exposure to allergens,

foods, drugs and xenobiotics [24].

PCD

Eukaryotic cells display two different ways to die:

necrosis and apoptosis, each with own peculiar mor-

phological and biochemical hallmarks. The former is

an accidental, passive and traumatic death, due to

catastrophic toxic events whereas the latter is a

genetically encoded physiological death required for

tissue and organ differentiation and development [26].

Furthermore, apoptosis, or programmed cell death

(PCD), is a fine regulated active process, also involved

in immunity, and whose morphological markers

include nuclear condensation and DNA fragmentation,production of reactive oxygen species, increased ion

leakage, cytochrome c release from mitochondria, and

caspase proteolytic activities [26, 27].

In plants, PCD takes place in an array of condi-

tions: during the development of root-tip cells, in the

differentiation of tracheal elements and lysigenous

aerenchyma, in the endosperm and aleurone layers of

the kernel. Also adverse environmental conditions

and biotic stresses, namely pollutant and pathogen


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attack, can promote PCD in plant [27]. In fact, the

hypersensitive response (HR) that may be triggered at

the attempted pathogen penetration site is a type of

PCD, frequently associated with the induction of

systemic immunity (SAR, systemic acquired resis-

tance) [28, 29]. In animal immune system, the main

role of apoptosis pertain to adaptive immunity,precisely in the restoration of homeostasis at the

end of an immune response, when, after lymphocyte

proliferation (clonal expansion), most of the progeny

of antigen-stimulated lymphocytes die by apoptosis,

leaving only functionally quiescent memory lympho-

cytes [14]. Otherwise, in animals, premature lysis of

the infected cells, due to apoptosis, can prevent the

complete multiplication of progeny virus if cells die

before virus multiplication, or when infected apopto-

tic cells are phagocytosed by macrophages [30].

Considering the fundamental role of HR-PCD inplant defence, it seems that, during the evolution,

plants implemented PCD more than animals did, as

an effective direct tool to improve their own defence

armamentarium.

RNAi

The RNA interference (RNAi) or post-transcriptional

gene silencing, based on the recognition and pro-

cessing of non-self double-stranded RNA (dsRNA) is

a defence mechanism against pathogenic nucleicacids [31]. Though this mechanism is conserved in all

eukaryotes, from the unicellular ones to mammals, it

seems not be involved in defence against fungal

pathogens.

Adaptive defence mechanisms

In vertebrates, adaptive immunity, also termed

specific or acquired immunity, adapts to a distinct

pathogen. It exhibits a tight specificity for foreign

(non-self) elicitors (antigens), being able to distin-

guish among different, even closely related, patho-

gens. Furthermore, adaptive immunity has the

ability to respond more vigorously to repeated

exposure to the same pathogen/antigen (immuno-

logical memory). The main weapons of thisimmune system are antibodies, secreted by B

lymphocytes and circulating in the blood (humoural

immunity), and T lymphocytes, able to either

destroy directly infected cells or activate phago-

cytes to kill pathogens (cell-mediated immunity,

Fig. 3) [6].

As above reported, plants lack adaptive immunity,

although they developed an alternative strategy to

fulfil an analogous need to survive from the pathogen

challenge. Traditionally, their defence mechanisms

can be activated by two distinct classes of elicitors.General elicitors, or PAMPs, induce non-host resis-

tance by PRRs-mediated recognition, whereas spe-

cific elicitors require a more specific system of

perception, leading to the host cultivar-specific

resistance. Specific elicitors are virulence factors

encoded by the avirulence (avr) genes of a given

pathogen race or strain, enabling it to overcome the

PAMP-triggered immunity. At the opposite side of

the barricade, cultivars of a given plant evolved a

strategy to counteract these specialized pathogens.

Therefore, the products of the plant resistance genes(R) ensure the perception of pathogen race/strain-

specific avr proteins, and the matching between pairs

of avr and R gene products, has been emphasized by

the gene-for-gene theory. Anyhow, either the host

surveillance strategies, i.e. PAMP-triggered (non-host

resistance) and the avr-induced (host resistance),

regardless of general or specific elicitors, constitute

two forms of the same innate immunity, in plants

(Fig. 3), being both PRRs and R proteins nonclonal

and germline-encoded [3234].

tsohnoNecnatsiser

etannIytinummi

aptivedA

ytinummi

tsoHecnatsiser

ecnatsiserlasaB

ytinummicificepSInnateimmunity

Fig. 3 The two subdivisions of plant innate immunity (non-

host and host resistance) are compared to animal innate and

adaptive immunity, respectively; the difference between basal

(or general) resistance and specific immunity are emphasized


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Autoimmunity

Due to adaptive immunity, animals experienced a

failure of the mechanisms normally responsible for

maintaining self-tolerance. Autoimmune diseases,

caused by abnormal immune responses directed

against self antigens (autoantigens), occur when

immature self-reactive T and B cells escape the

clonal deletion, an apoptotic cell death, and lympho-

cyte central tolerance is broken in thymus and bone

marrow, respectively. Furthermore, autoimmunity

may result from failure of mature T cell tolerance

in peripheral tissues, rather than in the generative

lymphoid organs [14].

In default of haematopoietic organs and immune

cells, plants overcome autoimmune disorders. How-

ever, if we consider autoimmunity as a general

deregulation of immune system, also plant may be

exposed to the detrimental effects of their own

defence strategies, such as those arising from fitness

costs. These are referred to as the trade off between

resources allocated for growth and reproduction and

disease resistance [7]. In plants, defence mechanisms

are highly expensive, from the metabolic point of

view. Due to their sessile habitus, plants are unable to

avoid the worsening environmental conditions, as

well as they cannot escape the plethora of the laying

before biotic stresses, thus, unlike animals, evolved

an huge number of different secondary metabolites

(i.e. phenilpropanoids, isoprenoids, alkaloids) to

overcome any danger. In this view, a diversion of

essential available resource, more than required, from

growth to defence, may occur in condition of low

pathogen pressure [7]. Moreover, as a consequence of

the shift between primary and secondary metabolism,

plants are faced with the problem of poisoning

enemies that are metabolically similar to their own,

such as insects and pathogens, sometimes incurring in

autotoxicity. Generally, plants avoid these side

effects by the compartmentalization of chemicals in

cell vacuoles, specialized organelles, nonplasmic or

extraplasmic compartments, or ad hoc secreting

tissues and organs such as glandular trichomes.

Besides, secondary compounds may occur in plant

cell as inactive precursors, becoming toxic by some

events during cell disturbance, when the precursors

and their hydrolizing enzymes come into contact in

the same compartment [35, 36].

Notwithstanding, a form of self perception may

also occur in plant, with the recognition of altered or

wrong self-structural components, such as oligoga-

lacturonides. These are able to trigger a general non-

host resistance, rather than an autoimmune disease,

although they cannot be strictly considered PAMPs.

Oligogalacturonides derive from the degradation of

homogalacturonan (polygalacturonic acid), the main

component of plant cell wall pectins, by fungal

polygalacturonases (PGs), whereas elicitor-active

oligogalacturonides (polymerization degree 810)

are produced by the modulation of PGs activity due

to plant polygalacturonase-inhibiting proteins

(PGIPs) [37].

Conclusions

In vertebrates, the adaptive immunity warrants the

specificity of the defence response, due to the ability

of generating a vast array of pathogen/antigen

specific receptors and clonal expansion of antigen

specific effector cells selected by receptor gene

rearrangement. On the contrary, innate immunity,

Table 1 Common and distinctive traits of animal and plant immunity (see text for details)

Characteristic Animal innate

immunity

Plant non-host resistance Animal adaptive immunity Plant host resistance

Receptors Nonclonal, encoded in

the germline

Nonclonal, encoded in

the germline

Clonal, rearranged during development

(somatic recombination)

Nonclonal, encoded in

the germline

Specificity No No Yes YesSelf tolerance Yes Yes/no (may induce non-

host resistance)

Yes/no (may induce autoimmune

disorders)

yes

Autoimmunity No ? Yes ?

Memory No No Yes ?


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either in plant and animal kingdom, activates

defences through a fixed number of germline encoded

PRRs that recognize highly conserved pathogen and

microbial components (PAMPs, more recently de-

fined MAMPs, microbial associated molecular pat-

terns) [6, 13, 38]. From this view, plants seem to lack

in a pathogen-specific immunity, at least in terms ofpathogen recognition. Indeed, as above mentioned,

cultivar-specific R proteins enable the recognition of

pathogen race/strain-specific avr proteins, i.e. effector

molecules specific to particular pathogens, fulfilling a

role similar to that of the adaptive immune systems in

animals. Nevertheless, the cultivar-pathogen race/

strain-specific (host) resistance has to be considered a

form of innate immunity, because of the similarities

between R proteins and PRRs. Possibly for this

reason, plants have many more innate immune

receptors than animals, either for basal (non-host)and host resistance [2, 33].

In conclusion, if on the one hand, plants and

animals differ in terms of adaptive immune response,

on the other hand, they conserved the same ability to

distinguish between general and specific pathogen

effectors (non-self), that is PAMPs/MAMPs and

antigens/avr proteins, respectively, although through

different mechanisms (Table 1). Therefore, the

enhanced specificity is the main selected trait of

immune response, responsible for the evolutionary

success of plants and animals.

Acknowledgements We are grateful to Dr. Giovanni Lodi

for providing Candida albicans micrograph. This study was

supported by the National Research Council, Plant Virology

Institute, U.O. Milan, DG.RSTL.107.

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