"Frontmatter". In: Plant Genomics and Proteomics

B
IOTIC
I
NTERACTIONS
Plants come into contact with a wide range of other organisms in their life-
time. These organisms can be beneficial, harmful, or neutral, and the plant
must be able to respond appropriately to each type. Thus plants have devel-
oped sophisticated mechanisms through which they respond to these organ-
isms. For example, how does the plant distinguish between a pathogenic
invasion and the establishment of a symbiotic relationship, and then respond
appropriately by excluding or destroying the former while guiding the
development of the latter? High-throughput genomics approaches have
made the global study of these responses possible. The added information
becoming available from the sequencing of the pathogen and symbiont
genomes will contribute to the development of a complete understanding of
the genes involved in the interactions. It is clear that in the interactions
between microbes and plants the same mechanisms are often used irrespec-
tive of whether the microbe is beneficial or pathogenic. However, the inte-
gration, timing and combinations of these mechanisms may result in the
different outcomes elicited by specific organisms. 
D
ISEASE
R
ESISTANCE
The original gene-for-gene disease resistance interaction in plants was
defined by Flor (1971) for the interaction between flax and its pathogen flax
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7. I
N T E R A C T I O N S W I T H T H E
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X T E R N A L
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N V I R O N M E N T

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rust. In this interaction the host and pathogen must have a pair of specific
alleles, one in each organism, for resistance to occur. The resistance gene (R)
in the plant and the corresponding avirulence gene (Avr) in the pathogen
are the basis of resistance, generally eliciting the hypersensitive response
(Table 7.1). The hypersensitive response occurs after the recognition of 
the pathogen by the plant with the induction of a cell death cascade in the
vicinity of the infection.
Disease resistance (R) genes and their homologs are among the most
prevalent genes in plant genomes (Meyers et al., 1999). These resistance
genes have been the subject of intense scrutiny over the past decade, and
many have been isolated. The isolated genes generally fall into five classes
(Hammond and Jones, 1997):
∑ The nucleotide binding (NBS)-leucine-rich repeat (LRR) genes 
∑ Detoxifying enzymes, e.g., the Hm1 gene in maize
∑ Intracellular serine/threonine protein kinases, e.g., the Pto gene in
tomato
∑ Extracellular LRR proteins with a single membrane spanning region
and short cytoplasmic carboxyl terminus, e.g., the cf9 gene in tomato
∑ Extracellular LRR proteins with a single membrane spanning region
and cytoplasmic kinase domain, e.g., the Xa21 gene in rice
The major class of these resistance genes is the NBS-LRR group, and this
group can be further subdivided into two subclasses (Jones, 2001):
∑ Those that carry amino-terminal homology to the Toll and Inter-
leukin-1 receptor (TIR) genes (the TIR-NBS-LRR family), e.g., the L
6
gene in flax
B
I O T I C
I
N T E R A C T I O N S
1 3 3
TABLE 7.1. T
HE
G
ENE
-
FOR
-G
ENE
I
NTERACTION
B
ETWEEN
P
LANT
R
ESISTANCE
G
ENES AND
P
ATHOGEN
A
VIRULENCE
G
ENES
. 
Plant Genes
Pathogen genes
R1
R2
Avr1
Hypersensitive response
No resistance, disease
Cell death
progression
Avr2
No resistance, disease progression
Hypersensitive response
Cell death
The presence of an interacting pair of genes results in the activation of the hypersensitive
response, leading to cell death. Other pairs of resistance and avirulence genes do not activate
the hypersensitive response and so result in disease progression.

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∑ Those that carry a putative coiled coil (CC) at their amino terminus
(the CC-NBS-LRR family), e.g., the RPS2 gene in Arabidopsis.
The structure of the R genes in these classes is shown in Figure 7.1. 
These R and Avr genes are shaped by a continuous evolutionary battle.
The plant R genes are believed to recognize the products of the pathogen
Avr genes and to activate the defense program (the hypersensitive response)
that prevents the pathogen from gaining a foothold. Because the Avr genes
prevent the colonization of the plant by the pathogen, selection should have
eliminated them unless they perform another essential function in the
pathogen, perhaps ensuring virulence in nonresistant plants. There is 
1 3 4
7. I
N T E R A C T I O N S W I T H T H E
E
X T E R N A L
E
N V I R O N M E N T
PM
NE
TM
TM
LRR
LRR
NBS
Kin
CC
CC
TIR
Nudeus
TIR
NBS
LRR
NLS
WRKY
Cytoplasm
RRS1-R
W
-Box
DNA
Apoplast
FIGURE 7.1.
Modular composition and predicted location of R protein classes. 
NBS-LRR proteins are predicted to encode cytoplasmic receptor molecules. RRS1-R
represents a novel NBS-LRR type that encodes a C-terminal NLS and a WRKY
domain. Presence of the WRKY DNA-binding domain suggests that RRS1-R activates
genes that are under the transcriptional control of W-box-containing promoters.
Abbreviations: CC, coiled-coil domain; Kin, kinase; LRR, leucine-rich repeat domain;
NBS, nucleotide-binding site; NE, nuclear envelope; NLS, nuclear localization signal;
PM, plasma membrane; TIR, Toll/interleukin-1-receptor; TM, transmembrane
domain. (Reprinted from Trends Plant Sci. 7, Lahaye, The Arabidopsis RRS1-R disease
resistance gene—uncovering the plant’s nucleus as the new battlefield of plant
defense, 425–427, Copyright 2002, with permission from Elsevier.)

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evidence of such a role for virus-encoded proteins that are recognized by
host R genes (Nimchuk et al., 2001). 
Recognition is considered to be the initial important event in the
response of plants to microbes. Many of the genes in the pathogen that are
responsible for both the invasion and the activation of defense responses are
thought to encode secreted proteins from the pathogen. One of the mecha-
nisms used by pathogens to deliver these proteins is a specialized secretion
system called the type III secretion system (TTSS), which delivers the bacte-
rial proteins directly into the host cell (Lugtenberg et al., 2002). This system
is widespread among both animal and plant pathogens and, as noted below,
may also play a role in symbiosis (Staskawicz and Parniske, 2001). There-
fore, the genomic sequences that are available from some pathogens can be
used with informatic tools to identify which of the open reading frames are
likely to be secreted proteins based on the structure of their leader sequences.
These proteins are primary targets for investigating the roles and interac-
tions between R and Avr genes. The identification of these relationships and
the roles of secreted proteins in the development of disease will be vital for
the development of new points of intervention in disease processes in crop
plants.
An understanding of the signal transduction networks by which the R
genes control the activation of defensive responses is of considerable inter-
est because the R genes are generally quite effective in preventing disease.
The use of Arabidopsis and the insertion mutants that are available has
thrown considerable light on these networks and the genes involved 
(Glazebrook, 2001). These data indicate that there are at least three distin-
guishable mechanisms through which gene-for-gene resistance can be medi-
ated. Some of the proposed interacting pathways are shown in Figure 7.2. 
Two of these pathways involve intermediate genes that have been iden-
tified, whereas the third does not yet have any identified required interme-
diates between the R gene and the resistance reaction. The genes involved
in mediating the resistance responses following the interaction of the R and
Avr gene products have the following properties, as shown by mutant
studies:
∑ NDR1—Required for non-race-specific resistance to bacterial and
fungal pathogens. It also mediates the systemic acquired resistance
(SAR) response. This gene can operate in both linear and parallel sig-
naling events, depending on the R gene function triggered (Tornero
et al., 2002). The Arabidopsis genome contains 28 genes with sequence
homology to the Arabidopsis NDR1 gene. Expression analysis of eight
of these genes identified two that show pathogen-dependent mRNA
accumulation (Varet et al., 2002). One of these two genes was also
expressed during infection with an avirulent oomycete, Peronospora