Comparative analysis of
host-pathogen interaction indicated that initially there is no difference on spore
germination, stomatal penetration and haustoria development by U. viciae-fabae on resistant and
susceptible genotypes of faba bean. The difference between resistant and
susceptible hosts started to appear post-sporulation, where resistant genotypes
continued to restrict sporulating uredia and infection hyphae. Fungal growth
was uniform in early infection, but least fungal growth (area of infection
sites and uredia) were observed in Doza#12034 during the advanced infection
stages. This explains the expression of the lowest IT 1C in Doza#12034 among
the faba bean genotypes. In contrast, the uredia development was not uniform
among the infection sites in Ac1655 resulting in different IT: 1 and 2. Both
resistant genotypes significantly suppressed fungal growth as compared to Fiord
both micro- and macroscopically without any evidence of cell death. This type
of rust resistance has also been observed in faba bean, earlier (Rashid
and Bernier 1986; Sillero et al. 2000). In contrast, some
studies also reported late hypersensitive cell death (Sillero
and Rubiales 2002), but this type of
resistance failed to insight immunity. Therefore, unlike cereals where
hypersensitivity is a hallmark of completely 
fungal growth in cereals (Ayliffe
et al. 2013b), the concept of hypersensitivity
is completely different in faba bean and the molecular basis underlying such resistance
type is still not well understood in faba bean.

            The variation in IT on field pea genotypes indicated the
existence of diversity in this host-pathogen system. Despite substantial fungal
growth occurring in plant tissue, uredia were less frequent and spread of IH
was restricted. As observed on faba bean, the resistance on field pea was also
incomplete (hypersensitive cell death was not apparent) under greenhouse
conditions as the rust pathogen sporulated on all resistant accessions.
Moreover, in comparison to faba bean resistant genotypes (Doza#12034 and
Ac1655), the number of uredia possessing infection sites were lower in field
pea. Barilli
et al. (2009b) reported field pea
seedlings were susceptible to Spanish, Syrian, Dutch and Australian U. viciae-fabae isolates under controlled
conditions, similar to these experiments on some field pea genotypes. In the
same study, field pea accessions grown under natural rust infection in Spain
showed field resistance (DS ranged 0-10). However, no natural rust infection in
field conditions has been observed on field pea in Australia (Lindbeck

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widespread rust occurrence on faba bean at many places in Australia, both faba
bean and field pea are grown side by side during the crop season and no
evidence of rust infection was observed on field pea (Pers. Comm. Adhikari).
However, rust infection was observed on the bottom leaves (no symptoms on top
leaves) of self-grown volunteer field pea plants within a rust infected faba bean
field (Pers. Comm. Ijaz). Therefore, it can be assumed that Australian field
pea cultivars carry field resistance genes against rust. It is also possible
that more favourable environmental conditions are required for the development
of rust on field pea than on faba bean. However, when we inoculated seven weeks
old field pea seedlings with U.
viciae-fabae pathotype 24-40 under greenhouse conditions (Ijaz et al.
Unpublished data) it showed resistant phenotype IT 2C with sporulation on all
leaves at flowering stage. This experiment was not carried further, but
concluded that sporulation occurred in adult plants of field pea. Therefore, a
comprehensive study is needed to examine the mechanism of infection in field
pea against faba bean rust in reference to seedling vs adult plant under
greenhouse vs field.

Among the reported
hosts, when lentil was challenged with faba bean rust, presence of IT flecks on
the leaf surface indicated host-pathogen recognition and auto-fluorescence
under microscopy indicated hypersensitive cell death in mesophyll cells
surrounding infection sites. This defence response prevented further fungal
growth completely. This type of complete resistance against faba bean rust in
lentil has also been reported by Negussie
et al. (2012). Thus, host-pathogen,
lentil-U. viciae-fabae is carrying a
compatible combination of major seedling rust resistance genes with their
corresponding avirulence effector genes against Australian pathotypes. In
addition, few infection sites showed pre-haustorial resistance where germinated
spores ceased growth before haustoria developed entirely a type of quantitative
resistance, often under the control of minor genes. Thus, it can be summarised
that lentil possessed both major and minor genes exhibiting pre- and
post-haustorial resistance against invading rust.

Chickpea showed no
macroscopic disease symptoms for both U.
viciae-fabae pathotypes, however, variation among infection sites were
visible microscopically. Despite significant growth occurring at some rust
infection sites, most infections were generally restricted, often confined to a
sub-stomatal vesicle with a few infection hyphae. Among larger infection sites,
some unique structural bodies (most likely to be immature uredia) were
observed, that looked similar in morphology to rust infection sites on Fiord
and Doza#12034 at 7 DAI. These infection sites, however, failed to sporulate
further because by the same time rust infected chickpea leaves had undergone
age dependant senescence, meaning that growth of the obligate biotrophic
pathogen could not continue.  Further
experiments were carried out to examine the fungal growth by maintaining the
chickpea plants under low temperature (18 oC) in greenhouse until 60
DAI, but no sporulation was observed.  Therefore,
some strong post-haustorial resistance mechanism is operational in chickpea
that is needed to be studied or explored in more details.  Ghimire
and Mansfield (1996) reported chickpea as a
non-host for U. viciae-fabae which
agrees with the findings of this study.

On lupin genotype Kiev
Mutant, macroscopic disease symptoms of rust infection showed immunity (no
sporulation) and microscopy identified larger infection sites with ceased
growth after producing infection hyphae following haustoria development.
Moreover, ceased fungal growth in small infection sites containing app only and
app+ssv were also seen during microscopy. Therefore, the pre- and
post-haustorial resistance is evident in lupin. No hypersensitive cell death
was observed in infected mesophyll cells, thus, for largely unknown reason, NHR
mechanism operates in genotype Kiev mutant against faba bean rust. In addition,
no fungal growth was observed in a narrow leaved genotype Jurien where necrotic
patches were visible against pathotype 63-63, when tested under microscope.
Therefore, Kiev mutant interacted with the fungus differently as compared to
all other tested lupin genotypes. These kinds of NH interactions have not been
observed before in lupin-faba bean rust pathosystem and further studies on the
mechanism of such interactions is needed.

Mung bean demonstrated a
typical NH resistance for faba bean rust pathogen. No significant fungal growth
occurred initially where appressorium failed to locate stomate, most likely
because of unknown physical or chemical factors. The frequency of haustoria
producing infections sites were very low, therefore remained undetected during
early growth stages, indicating sampling artefacts. Until now, mung bean – U. viciae-fabae was unknown and this is
the first study concluded mung bean a NH to faba bean rust pathogen.

In conclusion, macro-
and microscopic diversity of interactions among various host and NH legumes
infected with faba bean rust pathogen was demonstrated. It is generally known
that a probability of a pathogen infecting two plant genera in a habitat
decreases continuously in proportion to phylogenetic distance between these
genera (Gilbert
and Webb 2007). Three legumes V. faba, L. culinaris and P. sativum
tested in this study belonged to a single viceae
tribe (Choi
et al. 2004), thus during the
evolutionary course the rust pathogen U.
viciae-fabae acquired compatibility of reaction on these genera. In
contrast, chickpea was evolved in a separate tribe cicereae, but in close geographic vicinity. Therefore, the rust
pathogen showed significant growth inside mesophyll cells but failed to
completely parasitise on chickpea. In spite of possibility, mung bean and lupin
were evolved in very different tribes (Phaseoleae
and Genisteae, respectively), therefore, it responded apparently NHR response. Interestingly,
the haustoria containing infection sites were observed in all the tested
legumes, validating the ability of rust to extract nutrients from the plants
either host or NH at the initial stages. The fungal growth continues or ceases
only at the later stage depending upon the host type. Faba bean rust resistance
genes Uvf-2 and Uvf-3 derived from Doza#12034 and Ac1655, respectively, are not
associated with early or late hypersensitivity (no autofluorescence was
detected under UV light). Thus, these resistance genes expressed incomplete
resistance types in faba bean against rust. Among the host range for Australian
faba bean rust pathogen, faba bean and field pea were complete host carrying
diversity in seedling resistance, lentil as the resistant host expressing
complete resistance (hypersensitivity), but chickpea, lupin and mung bean were
categorised as NH. Thus, in addition to faba bean, any resistance breakdown by
the evolution of virulence in U.
viciae-fabae pathotypes has the potential of causing crop failure in field
pea and lentil in Australia.

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