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The molecular basis of plant resistance and
defense responses to pathogens: Current status




            Sruthi.N
Introduction

   Many plant-associated microbes are pathogens that impair plant
    growth and reproduction

   Pathogens may proliferate in intercellular spaces (the apoplast)
    after entering through stomata or hydathodes (bacteria), enter
    plant epidermal cells, or extend hyphae onto the plant cells
    (fungi)

   Innate immune receptors in plants detect the presence of
    microbial pathogens and trigger defense responses to terminate
    or restrict pathogen growth
Elicitors of defence responses


   Any substance that has the capability of activating defense
    responses in plants
   Include components of the cell surface as well as excreted
    metabolites
                         Elicitors


      General                          Race specific
    a) Oligosaccharide elicitors      a)avr gene products
    b) Protein/peptide elicitors
                                                   (Ebel et al.,1998)
Perception of elicitor signals

   Binding proteins:

   Oligosaccharide-binding sites:
    -Specific glucan-binding sites on soybean root plasma
    membranes
    -high-affinity binding sites for chitin fragments in tomato, rice

   Glycopeptide- and peptide-binding sites:
    -Binding sites for peptidoglycans have been identified in wheat
    plasma membranes
Plant defense to pathogens


•   Plants respond to infection using a two-branched innate
    immune system

    -Recognition and response to molecules common to many
      classes of microbes (basal disease resistance)

    -Response to pathogen virulence factors

                                               (Liu et al.,2008)
Basal defense


   Triggered by trans-membrane receptors that recognize
    conserved molecules released by a variety of (unrelated)
    microbes

   Include cell wall fragments, chitin or peptide motifs in bacterial
    flagella - PAMPs or MAMPs

   PAMP- triggered immunity (PTI)
                                                     (Liu et al.,2008)
Secondary defense response



   Against virulence effector proteins produced by pathogens

   Effector –triggered immunity (ETI)

   Mediated by resistance (R) proteins



                                                (Liu et al., 2008)
Phases of pathogen-triggered immunity




                               (Chisholm et al.,2006)
Concepts regarding pathogen recognition and defense




   Gene-for-gene resistance (Flor , 1947)

   Guard hypothesis (Beizen et al.,1998)
Gene-for-gene resistance


   For resistance to occur, complementary pairs of dominant genes,
    one in the host and the other in the pathogen, are required
    (incompatibility)

   A loss or alteration to either the plant resistance (R) gene or the
    pathogen avirulence (Avr) gene leads to disease (compatibility)


                                               (Hammond-Kosack et al., 1997)
Types of genetic interactions between plants and
             pathogenic microbes




                          (Hammond-Kosack et al., 1997)
Plant disease resistance genes


   Encode proteins that recognize Avr-gene-dependent ligands

   Activate signaling cascade(s) that coordinate the initial plant
    defense responses to impair pathogen ingress

   Capacity for rapid evolution of specificity

   Common feature of resistance proteins is a leucine-rich repeat

                                     (Hammond-Kosack et al., 1997)
Classes of resistance proteins




                                 (Chisholm et al.,2006)
Extracellular LRR class of R genes

   Have classic receptor-kinase formats - an extracelluar LRR, a
    membrane spanning region and an intracellular protein kinase
    domain

   Against pathogens that have an extracellular lifestyle

   Examples: rice Xa21 against Xanthomonas, cf genes of tomato
    against Cladosporium fulvum.
NB-LRR R proteins


   Consists of four domains connected by linkers

   A leucine-rich repeat domain (LRR) fused to a nucleotide binding
    (NB) domain

   NB-LRR core equipped with variable amino- and carboxy-terminal
    domains

                                               (Tameling et al., 2008)
NB-LRR subfamilies


   TIR NB-LRRs (Toll/interleukin-1 receptor like NB-LRRs)

   CC-NB-LRRs (Coiled Coil NB-LRRs)
      Solanaceous domain (SD)

      BED zinc finger DNA-binding domain




                                            (Tameling et al.,2008)
Domains found in plant LRR R proteins




                                    (Tameling et al.,2008)
Deviations from gene-for-gene concept


   One R gene may confer specificity to more than one ligand
     - RPM1 in Arabidopsis confers resistance against P.syringae
        expressing either avrRpm1 and avrB

   More than one R gene may exist for a given Avr gene
     - Pto and Prf genes encode biochemically distinct components
        of the same pathway
     - Two genes at the Cf-2 locus furnish identical functions

                                                      (Bent, 1996)
Guard hypothesis


    Key points

d)   An effector acting as a virulence factor has a target(s) in the host

f)   By manipulating or altering this target(s) the effector contributes to
     pathogen success in susceptible host genotypes

h)   Effector perturbation of a host target generates a “pathogen induced
     modified self” molecular pattern, which activates the corresponding
     NB-LRR protein, leading to ETI

                                                      (Jones et al.,2006)
Guard hypothesis




                   (Jones et al.,2006)
Plant defense responses

   Hypersensitive response

   Production of reactive oxygen species

   Cell wall fortification

   Production of antimicrobial metabolites (phytoalexins)

   Defense signal transduction

   Synthesis of enzymes harmful to pathogen (eg. chitinases,
    glucanases)                               (Nurnberger et al.,2006)
Types of activated defense responses




(A) Hypersensitive response in single lettuce mesophyll cells penetrated by haustoria of an incompatible isolate of
the biotrophic fungus Bremia lactucae B) H2O2 generation in lettuce cell walls, in the vicinity of the incompatible
bacterium P. syringae pv phaseolicola(C) Papillae formation. Papillae develop beneath the penetration peg (PP)
and germinating spore (S) of an avirulent isolate of the biotrophic fungusErysiphe graminis f sp hordei on barley
leaves expressing the Mlg gene.



                                                                   (Hammond-Kosack et al., 1997)
Defense signaling pathways

     SA-dependant signaling

   Effective against biotrophic pathogens

   Activated by the initiation of HR in plants

   Rise in SA levels            dissociation of NPR1 oligomers to
    monomers            interaction with TGA-type transcription factors
                activation of PR gene expression

   TGAs 2,5, and 6 and WRKY70 required for full expression of PR-1
                                                      (Glazebrook, 2005)
Defense signaling pathways
       JA- and ET- dependent signaling

    Effective against necrotrophic pathogens

    Increase in JA levels and induction of effector genes (PDF1.2, VSP1)

    Induction of transcription factors ERF1, RAP2.6 and JIN1 which
     activates many defense related genes

    Some JA regulated genes also regulated by ET (PDF1.2 , ERF1)
                                                       (Glazebrook, 2005)
Defense signaling pathways

    JA- and ET- dependent signaling

   JA levels regulated by cellulose synthases

   JAR1 involved in conversion of JA to active form by conjugation with
    amino acids like isoleucine

   In Arabidopsis, all activities of JA requires the function of CO11.

   Some responses to JA require the function of an MAP kinase
    encoded by MPK4
                                                       (Glazebrook, 2005)
Defense signaling pathways


    Cross-talk between SA and JA/ET signaling

   Helps the plant to minimize energy costs and create a flexible
    signaling network that allows the plant to finely tune its defense
    response to the invaders encountered

   Most reports indicate a mutually antagonistic interaction between
    SA- and JA dependent signaling.

                                                      (Koornneef et al., 2008)
Molecular players in SA/JA crosstalk


   NPR1, required for transduction of SA signaling is a suppressor of
    JA response

   Expression of GRX480 is SA inducible and dependent on NPR1

   Overexpression of GRX480 completely abolished MeJA-induced
    PDF1.2 expression, but does not affect the induction of the JA-
    responsive genes LOX2 and VSP2


                                                (Koornneef et al., 2008)
Molecular players in SA/JA crosstalk



   Overexpression of WRKY70 caused enhanced expression of SA-
    responsive PR genes and suppressed methyl jasmonate (MeJA)-
    induced expression of PDF1.2

   MPK4 is a negative regulator of SA signaling and a positive
    regulator of JA signaling in Arabidopsis

                                          (Koornneef et al., 2008)
PR proteins

   Coded by host plants as a response to pathological or related
    situations

   Accumulate not only locally in the place of infection, formed
    systemically following infection by pathogens.

   Wide array of functions: hydrolases, transcription factors,
    protease inhibitors etc.
                                                      (Scherer et
    al.,2005)
Classes of PR proteins




                         (Scherer et al.,2005)
Non-Host Resistance


    Two mechanisms
   In case of a potentially new host, pathogen’s effectors could be
    ineffective, resulting in little or no supression of PTI, and failure
    of pathogen growth

   One or more of the effector complement of the would-be
    pathogen could be recognized by the NB-LRR proteins of plants
    other than it’s coadapted host , resulting in ETI

   Arabidopsis resistance to non-adapted powdery mildew Blumeria
    graminis f. sp. hordei
                                                         (Jones et al., 2006)
Arabidopsis Nonhost Resistance
            to Bgh




                                 (Ellis, 2006)
How R genes initiate defense signaling pathways
   R proteins recognize pathogen effectors in the cytoplasm

   Effector perception may result in altered intra and inter-molecular R
    protein interactions, including oligomerization.

   Activated R proteins cycle into the nucleus and directly bind
    transcriptional repressors of innate immunity, resulting in
    transcriptional reprogramming of the plant cell

   Studies conducted for N, MLA,RPS4, and RX
                                                  (Liu et al., 2008)
Nuclear activity of MLA immune receptors




                                      (Liu et al., 2008)
Molecular basis of plant resistance and defense responses to pathogens
Objective of the study


   Study of the interaction of tomato plants with tomato powdery
    mildew fungus, Oidium neolycopersici

   The monogenic genes Ol-1, ol-2 and Ol-4 confer resistance to
    tomato powdery mildew Oidium neolycopersici via different
    mechanisms

   Study of the molecular and biochemical mechanisms involved
Main interaction stages in compatible and incompatible
interactions
H2O2 and callose accumulation in compatible and
           incompatible interactions
Different expression classes of the DE-TDF in cDNA AFLP
                         analysis
BLAST Results
RT-PCR
Conclusion of the study

   ROS, callose accumulation, and upregulation of DE-TDF
    associated with resistances conferred by dominant and recessive
    Ol genes

   cDNA – AFLP profiling clarified that 81% of upregulated DE-TDF
    are common for both compatible and incompatible interactions

   Class III DE-TDF were up regulated only in incompatible
    interactions and are specific for specific resistance genes

   DE-TDF profiles of NIL-OL-1 and NIL-OL-4 deviated much but
    similarities were observed between NIL-OL-1 and F3-ol-2
Conclusion




        An evolutionary arms race..
Discussion
THANK U…

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Molecular basis of plant resistance and defense responses to pathogens

  • 1. The molecular basis of plant resistance and defense responses to pathogens: Current status Sruthi.N
  • 2. Introduction  Many plant-associated microbes are pathogens that impair plant growth and reproduction  Pathogens may proliferate in intercellular spaces (the apoplast) after entering through stomata or hydathodes (bacteria), enter plant epidermal cells, or extend hyphae onto the plant cells (fungi)  Innate immune receptors in plants detect the presence of microbial pathogens and trigger defense responses to terminate or restrict pathogen growth
  • 3. Elicitors of defence responses  Any substance that has the capability of activating defense responses in plants  Include components of the cell surface as well as excreted metabolites Elicitors General Race specific a) Oligosaccharide elicitors a)avr gene products b) Protein/peptide elicitors (Ebel et al.,1998)
  • 4. Perception of elicitor signals  Binding proteins:  Oligosaccharide-binding sites: -Specific glucan-binding sites on soybean root plasma membranes -high-affinity binding sites for chitin fragments in tomato, rice  Glycopeptide- and peptide-binding sites: -Binding sites for peptidoglycans have been identified in wheat plasma membranes
  • 5. Plant defense to pathogens • Plants respond to infection using a two-branched innate immune system -Recognition and response to molecules common to many classes of microbes (basal disease resistance) -Response to pathogen virulence factors (Liu et al.,2008)
  • 6. Basal defense  Triggered by trans-membrane receptors that recognize conserved molecules released by a variety of (unrelated) microbes  Include cell wall fragments, chitin or peptide motifs in bacterial flagella - PAMPs or MAMPs  PAMP- triggered immunity (PTI) (Liu et al.,2008)
  • 7. Secondary defense response  Against virulence effector proteins produced by pathogens  Effector –triggered immunity (ETI)  Mediated by resistance (R) proteins (Liu et al., 2008)
  • 8. Phases of pathogen-triggered immunity (Chisholm et al.,2006)
  • 9. Concepts regarding pathogen recognition and defense  Gene-for-gene resistance (Flor , 1947)  Guard hypothesis (Beizen et al.,1998)
  • 10. Gene-for-gene resistance  For resistance to occur, complementary pairs of dominant genes, one in the host and the other in the pathogen, are required (incompatibility)  A loss or alteration to either the plant resistance (R) gene or the pathogen avirulence (Avr) gene leads to disease (compatibility) (Hammond-Kosack et al., 1997)
  • 11. Types of genetic interactions between plants and pathogenic microbes (Hammond-Kosack et al., 1997)
  • 12. Plant disease resistance genes  Encode proteins that recognize Avr-gene-dependent ligands  Activate signaling cascade(s) that coordinate the initial plant defense responses to impair pathogen ingress  Capacity for rapid evolution of specificity  Common feature of resistance proteins is a leucine-rich repeat (Hammond-Kosack et al., 1997)
  • 13. Classes of resistance proteins (Chisholm et al.,2006)
  • 14. Extracellular LRR class of R genes  Have classic receptor-kinase formats - an extracelluar LRR, a membrane spanning region and an intracellular protein kinase domain  Against pathogens that have an extracellular lifestyle  Examples: rice Xa21 against Xanthomonas, cf genes of tomato against Cladosporium fulvum.
  • 15. NB-LRR R proteins  Consists of four domains connected by linkers  A leucine-rich repeat domain (LRR) fused to a nucleotide binding (NB) domain  NB-LRR core equipped with variable amino- and carboxy-terminal domains (Tameling et al., 2008)
  • 16. NB-LRR subfamilies  TIR NB-LRRs (Toll/interleukin-1 receptor like NB-LRRs)  CC-NB-LRRs (Coiled Coil NB-LRRs)  Solanaceous domain (SD)  BED zinc finger DNA-binding domain (Tameling et al.,2008)
  • 17. Domains found in plant LRR R proteins (Tameling et al.,2008)
  • 18. Deviations from gene-for-gene concept  One R gene may confer specificity to more than one ligand - RPM1 in Arabidopsis confers resistance against P.syringae expressing either avrRpm1 and avrB  More than one R gene may exist for a given Avr gene - Pto and Prf genes encode biochemically distinct components of the same pathway - Two genes at the Cf-2 locus furnish identical functions (Bent, 1996)
  • 19. Guard hypothesis  Key points d) An effector acting as a virulence factor has a target(s) in the host f) By manipulating or altering this target(s) the effector contributes to pathogen success in susceptible host genotypes h) Effector perturbation of a host target generates a “pathogen induced modified self” molecular pattern, which activates the corresponding NB-LRR protein, leading to ETI (Jones et al.,2006)
  • 20. Guard hypothesis (Jones et al.,2006)
  • 21. Plant defense responses  Hypersensitive response  Production of reactive oxygen species  Cell wall fortification  Production of antimicrobial metabolites (phytoalexins)  Defense signal transduction  Synthesis of enzymes harmful to pathogen (eg. chitinases, glucanases) (Nurnberger et al.,2006)
  • 22. Types of activated defense responses (A) Hypersensitive response in single lettuce mesophyll cells penetrated by haustoria of an incompatible isolate of the biotrophic fungus Bremia lactucae B) H2O2 generation in lettuce cell walls, in the vicinity of the incompatible bacterium P. syringae pv phaseolicola(C) Papillae formation. Papillae develop beneath the penetration peg (PP) and germinating spore (S) of an avirulent isolate of the biotrophic fungusErysiphe graminis f sp hordei on barley leaves expressing the Mlg gene. (Hammond-Kosack et al., 1997)
  • 23. Defense signaling pathways SA-dependant signaling  Effective against biotrophic pathogens  Activated by the initiation of HR in plants  Rise in SA levels dissociation of NPR1 oligomers to monomers interaction with TGA-type transcription factors activation of PR gene expression  TGAs 2,5, and 6 and WRKY70 required for full expression of PR-1 (Glazebrook, 2005)
  • 24. Defense signaling pathways JA- and ET- dependent signaling  Effective against necrotrophic pathogens  Increase in JA levels and induction of effector genes (PDF1.2, VSP1)  Induction of transcription factors ERF1, RAP2.6 and JIN1 which activates many defense related genes  Some JA regulated genes also regulated by ET (PDF1.2 , ERF1) (Glazebrook, 2005)
  • 25. Defense signaling pathways JA- and ET- dependent signaling  JA levels regulated by cellulose synthases  JAR1 involved in conversion of JA to active form by conjugation with amino acids like isoleucine  In Arabidopsis, all activities of JA requires the function of CO11.  Some responses to JA require the function of an MAP kinase encoded by MPK4 (Glazebrook, 2005)
  • 26. Defense signaling pathways Cross-talk between SA and JA/ET signaling  Helps the plant to minimize energy costs and create a flexible signaling network that allows the plant to finely tune its defense response to the invaders encountered  Most reports indicate a mutually antagonistic interaction between SA- and JA dependent signaling. (Koornneef et al., 2008)
  • 27. Molecular players in SA/JA crosstalk  NPR1, required for transduction of SA signaling is a suppressor of JA response  Expression of GRX480 is SA inducible and dependent on NPR1  Overexpression of GRX480 completely abolished MeJA-induced PDF1.2 expression, but does not affect the induction of the JA- responsive genes LOX2 and VSP2 (Koornneef et al., 2008)
  • 28. Molecular players in SA/JA crosstalk  Overexpression of WRKY70 caused enhanced expression of SA- responsive PR genes and suppressed methyl jasmonate (MeJA)- induced expression of PDF1.2  MPK4 is a negative regulator of SA signaling and a positive regulator of JA signaling in Arabidopsis (Koornneef et al., 2008)
  • 29. PR proteins  Coded by host plants as a response to pathological or related situations  Accumulate not only locally in the place of infection, formed systemically following infection by pathogens.  Wide array of functions: hydrolases, transcription factors, protease inhibitors etc. (Scherer et al.,2005)
  • 30. Classes of PR proteins (Scherer et al.,2005)
  • 31. Non-Host Resistance Two mechanisms  In case of a potentially new host, pathogen’s effectors could be ineffective, resulting in little or no supression of PTI, and failure of pathogen growth  One or more of the effector complement of the would-be pathogen could be recognized by the NB-LRR proteins of plants other than it’s coadapted host , resulting in ETI  Arabidopsis resistance to non-adapted powdery mildew Blumeria graminis f. sp. hordei (Jones et al., 2006)
  • 32. Arabidopsis Nonhost Resistance to Bgh (Ellis, 2006)
  • 33. How R genes initiate defense signaling pathways  R proteins recognize pathogen effectors in the cytoplasm  Effector perception may result in altered intra and inter-molecular R protein interactions, including oligomerization.  Activated R proteins cycle into the nucleus and directly bind transcriptional repressors of innate immunity, resulting in transcriptional reprogramming of the plant cell  Studies conducted for N, MLA,RPS4, and RX (Liu et al., 2008)
  • 34. Nuclear activity of MLA immune receptors (Liu et al., 2008)
  • 36. Objective of the study  Study of the interaction of tomato plants with tomato powdery mildew fungus, Oidium neolycopersici  The monogenic genes Ol-1, ol-2 and Ol-4 confer resistance to tomato powdery mildew Oidium neolycopersici via different mechanisms  Study of the molecular and biochemical mechanisms involved
  • 37. Main interaction stages in compatible and incompatible interactions
  • 38. H2O2 and callose accumulation in compatible and incompatible interactions
  • 39. Different expression classes of the DE-TDF in cDNA AFLP analysis
  • 42. Conclusion of the study  ROS, callose accumulation, and upregulation of DE-TDF associated with resistances conferred by dominant and recessive Ol genes  cDNA – AFLP profiling clarified that 81% of upregulated DE-TDF are common for both compatible and incompatible interactions  Class III DE-TDF were up regulated only in incompatible interactions and are specific for specific resistance genes  DE-TDF profiles of NIL-OL-1 and NIL-OL-4 deviated much but similarities were observed between NIL-OL-1 and F3-ol-2
  • 43. Conclusion An evolutionary arms race..