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Nonhost resistance to rust pathogens - a continuation of continua.

Bettgenhaeuser J, Gilbert B, Ayliffe M, Moscou MJ - Front Plant Sci (2014)

Bottom Line: Delimiting the boundary between host and nonhost has been complicated by the quantitative nature of phenotypes in the transition between these two states.This leads to a continuum of disease phenotypes in the interaction with different plant species, observed as a range from compatibility (host) to complete immunity within a species (nonhost).In this review we will highlight how the quantitative nature of disease resistance in these intermediate interactions is caused by a continuum of defense barriers, which a pathogen needs to overcome for successfully establishing itself in the host.

View Article: PubMed Central - PubMed

Affiliation: The Sainsbury Laboratory, Norwich Research Park Norwich, UK.

ABSTRACT
The rust fungi (order: Pucciniales) are a group of widely distributed fungal plant pathogens, which can infect representatives of all vascular plant groups. Rust diseases significantly impact several crop species and considerable research focuses on understanding the basis of host specificity and nonhost resistance. Like many pathogens, rust fungi vary considerably in the number of hosts they can infect, such as wheat leaf rust (Puccinia triticina), which can only infect species in the genera Triticum and Aegilops, whereas Asian soybean rust (Phakopsora pachyrhizi) is known to infect over 95 species from over 42 genera. A greater understanding of the genetic basis determining host range has the potential to identify sources of durable resistance for agronomically important crops. Delimiting the boundary between host and nonhost has been complicated by the quantitative nature of phenotypes in the transition between these two states. Plant-pathogen interactions in this intermediate state are characterized either by (1) the majority of accessions of a species being resistant to the rust or (2) the rust only being able to partially complete key components of its life cycle. This leads to a continuum of disease phenotypes in the interaction with different plant species, observed as a range from compatibility (host) to complete immunity within a species (nonhost). In this review we will highlight how the quantitative nature of disease resistance in these intermediate interactions is caused by a continuum of defense barriers, which a pathogen needs to overcome for successfully establishing itself in the host. To illustrate continua as this underlying principle, we will discuss the advances that have been made in studying nonhost resistance towards rust pathogens, particularly cereal rust pathogens.

No MeSH data available.


Related in: MedlinePlus

Microscopic analyses of NHR outcomes to rust pathogens. (A) Growth of a Melampsora lini (flax rust) germ tube on the surface of a rice leaf. An aberrant appressorium-like structure (al) has been produced. (B) Pre-haustorial resistance against a Puccinia graminis f. sp. tritici infection site on Setaria italica. Contact of a fungal infection hyphae with a single mesophyll cell results in autofluorescence. (C,D) An autofluorescent Brachypodium distachyon mesophyll cell (C) containing a Puccinia striiformis f. sp. tritici haustorium (D). (E) A Puccinia hordei infection site on rice with a single, non-autofluorescent mesophyll cell containing a haustorium. (F,G) A Puccinia striiformis f. sp. tritici urediniospore on the surface of a rice leaf that has produced an appressorium (F) and underlying infection hyphae (G) that encompass multiple mesophyll cells. (H) A Puccinia graminis f. sp. tritici infection site on a rice leaf producing infection hyphae that encompass numerous mesophyll cells. Each dark, circular structure surrounded by green stained fungal infection hyphae is a single mesophyll cell. (I) Multiple Puccinia striiformis f. sp. tritici uredinia on a Brachypodium distachyon leaf producing urediniospores with underlying infection hyphae also apparent. af, autofluorescent plant cell; gt, spore germ tube; ifh, infection hyphae; h, haustoria; ssv, substomatal vesicle; u, urediniospore. All microscopic images were produced as described by Ayliffe et al. (2011).
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Figure 2: Microscopic analyses of NHR outcomes to rust pathogens. (A) Growth of a Melampsora lini (flax rust) germ tube on the surface of a rice leaf. An aberrant appressorium-like structure (al) has been produced. (B) Pre-haustorial resistance against a Puccinia graminis f. sp. tritici infection site on Setaria italica. Contact of a fungal infection hyphae with a single mesophyll cell results in autofluorescence. (C,D) An autofluorescent Brachypodium distachyon mesophyll cell (C) containing a Puccinia striiformis f. sp. tritici haustorium (D). (E) A Puccinia hordei infection site on rice with a single, non-autofluorescent mesophyll cell containing a haustorium. (F,G) A Puccinia striiformis f. sp. tritici urediniospore on the surface of a rice leaf that has produced an appressorium (F) and underlying infection hyphae (G) that encompass multiple mesophyll cells. (H) A Puccinia graminis f. sp. tritici infection site on a rice leaf producing infection hyphae that encompass numerous mesophyll cells. Each dark, circular structure surrounded by green stained fungal infection hyphae is a single mesophyll cell. (I) Multiple Puccinia striiformis f. sp. tritici uredinia on a Brachypodium distachyon leaf producing urediniospores with underlying infection hyphae also apparent. af, autofluorescent plant cell; gt, spore germ tube; ifh, infection hyphae; h, haustoria; ssv, substomatal vesicle; u, urediniospore. All microscopic images were produced as described by Ayliffe et al. (2011).

Mentions: A rust that is capable of parasitizing a plant species is said to be an adapted pathogen of that species, i.e., it can form all the necessary cellular components for colonization and successful reproduction. This same rust species will be incapable of parasitizing the vast majority of plant species for which it is a nonadapted pathogen. Infection of a host plant by urediniospores from an adapted rust pathogen in many cases involves germination of the spore on the leaf surface and growth of a germ tube across the leaf surface, whereupon it identifies a plant stoma by a thigmotropic response, leading to the production of an appressorium over the stoma (Figures 1D and 2F). (Note: although Figures 1 and 2 depict NHR outcomes the same fungal structures are produced during host infection.) From the appressorium an infection peg is inserted between the stomatal guard cells and a substomatal vesicle is produced within the leaf apoplast. Some rust species (e.g., Phakopsora pachyrizi) enter the host plant by germinated urediniospores forming an appressorium on the leaf surface and directly penetrating through the plant epidermis with an appressorium, and subsequently the hypha infect intercellular space. Infection of the alternate hosts of cereal rusts is also performed in this latter manner.


Nonhost resistance to rust pathogens - a continuation of continua.

Bettgenhaeuser J, Gilbert B, Ayliffe M, Moscou MJ - Front Plant Sci (2014)

Microscopic analyses of NHR outcomes to rust pathogens. (A) Growth of a Melampsora lini (flax rust) germ tube on the surface of a rice leaf. An aberrant appressorium-like structure (al) has been produced. (B) Pre-haustorial resistance against a Puccinia graminis f. sp. tritici infection site on Setaria italica. Contact of a fungal infection hyphae with a single mesophyll cell results in autofluorescence. (C,D) An autofluorescent Brachypodium distachyon mesophyll cell (C) containing a Puccinia striiformis f. sp. tritici haustorium (D). (E) A Puccinia hordei infection site on rice with a single, non-autofluorescent mesophyll cell containing a haustorium. (F,G) A Puccinia striiformis f. sp. tritici urediniospore on the surface of a rice leaf that has produced an appressorium (F) and underlying infection hyphae (G) that encompass multiple mesophyll cells. (H) A Puccinia graminis f. sp. tritici infection site on a rice leaf producing infection hyphae that encompass numerous mesophyll cells. Each dark, circular structure surrounded by green stained fungal infection hyphae is a single mesophyll cell. (I) Multiple Puccinia striiformis f. sp. tritici uredinia on a Brachypodium distachyon leaf producing urediniospores with underlying infection hyphae also apparent. af, autofluorescent plant cell; gt, spore germ tube; ifh, infection hyphae; h, haustoria; ssv, substomatal vesicle; u, urediniospore. All microscopic images were produced as described by Ayliffe et al. (2011).
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4263244&req=5

Figure 2: Microscopic analyses of NHR outcomes to rust pathogens. (A) Growth of a Melampsora lini (flax rust) germ tube on the surface of a rice leaf. An aberrant appressorium-like structure (al) has been produced. (B) Pre-haustorial resistance against a Puccinia graminis f. sp. tritici infection site on Setaria italica. Contact of a fungal infection hyphae with a single mesophyll cell results in autofluorescence. (C,D) An autofluorescent Brachypodium distachyon mesophyll cell (C) containing a Puccinia striiformis f. sp. tritici haustorium (D). (E) A Puccinia hordei infection site on rice with a single, non-autofluorescent mesophyll cell containing a haustorium. (F,G) A Puccinia striiformis f. sp. tritici urediniospore on the surface of a rice leaf that has produced an appressorium (F) and underlying infection hyphae (G) that encompass multiple mesophyll cells. (H) A Puccinia graminis f. sp. tritici infection site on a rice leaf producing infection hyphae that encompass numerous mesophyll cells. Each dark, circular structure surrounded by green stained fungal infection hyphae is a single mesophyll cell. (I) Multiple Puccinia striiformis f. sp. tritici uredinia on a Brachypodium distachyon leaf producing urediniospores with underlying infection hyphae also apparent. af, autofluorescent plant cell; gt, spore germ tube; ifh, infection hyphae; h, haustoria; ssv, substomatal vesicle; u, urediniospore. All microscopic images were produced as described by Ayliffe et al. (2011).
Mentions: A rust that is capable of parasitizing a plant species is said to be an adapted pathogen of that species, i.e., it can form all the necessary cellular components for colonization and successful reproduction. This same rust species will be incapable of parasitizing the vast majority of plant species for which it is a nonadapted pathogen. Infection of a host plant by urediniospores from an adapted rust pathogen in many cases involves germination of the spore on the leaf surface and growth of a germ tube across the leaf surface, whereupon it identifies a plant stoma by a thigmotropic response, leading to the production of an appressorium over the stoma (Figures 1D and 2F). (Note: although Figures 1 and 2 depict NHR outcomes the same fungal structures are produced during host infection.) From the appressorium an infection peg is inserted between the stomatal guard cells and a substomatal vesicle is produced within the leaf apoplast. Some rust species (e.g., Phakopsora pachyrizi) enter the host plant by germinated urediniospores forming an appressorium on the leaf surface and directly penetrating through the plant epidermis with an appressorium, and subsequently the hypha infect intercellular space. Infection of the alternate hosts of cereal rusts is also performed in this latter manner.

Bottom Line: Delimiting the boundary between host and nonhost has been complicated by the quantitative nature of phenotypes in the transition between these two states.This leads to a continuum of disease phenotypes in the interaction with different plant species, observed as a range from compatibility (host) to complete immunity within a species (nonhost).In this review we will highlight how the quantitative nature of disease resistance in these intermediate interactions is caused by a continuum of defense barriers, which a pathogen needs to overcome for successfully establishing itself in the host.

View Article: PubMed Central - PubMed

Affiliation: The Sainsbury Laboratory, Norwich Research Park Norwich, UK.

ABSTRACT
The rust fungi (order: Pucciniales) are a group of widely distributed fungal plant pathogens, which can infect representatives of all vascular plant groups. Rust diseases significantly impact several crop species and considerable research focuses on understanding the basis of host specificity and nonhost resistance. Like many pathogens, rust fungi vary considerably in the number of hosts they can infect, such as wheat leaf rust (Puccinia triticina), which can only infect species in the genera Triticum and Aegilops, whereas Asian soybean rust (Phakopsora pachyrhizi) is known to infect over 95 species from over 42 genera. A greater understanding of the genetic basis determining host range has the potential to identify sources of durable resistance for agronomically important crops. Delimiting the boundary between host and nonhost has been complicated by the quantitative nature of phenotypes in the transition between these two states. Plant-pathogen interactions in this intermediate state are characterized either by (1) the majority of accessions of a species being resistant to the rust or (2) the rust only being able to partially complete key components of its life cycle. This leads to a continuum of disease phenotypes in the interaction with different plant species, observed as a range from compatibility (host) to complete immunity within a species (nonhost). In this review we will highlight how the quantitative nature of disease resistance in these intermediate interactions is caused by a continuum of defense barriers, which a pathogen needs to overcome for successfully establishing itself in the host. To illustrate continua as this underlying principle, we will discuss the advances that have been made in studying nonhost resistance towards rust pathogens, particularly cereal rust pathogens.

No MeSH data available.


Related in: MedlinePlus