Mechanisms of Wheat Resistance to Leaf Rust: History
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Subjects: Plant Sciences
Contributor:
Johannes Mapuranga
,
Jiaying Chang
,
Jiaojie Zhao
,
Maili Liang
,
Ruolin Li
,
Yanhui Wu
,
Na Zhang
,
Lirong Zhang
,
Wenxiang Yang

Wheat leaf rust, caused by the obligate biotrophic fungus Puccinia triticina Eriks. (Pt), is one of the most common wheat foliar diseases that continuously threatens global wheat production. Currently, the approaches used to mitigate pathogen infestation include the application of fungicides and the deployment of resistance genes or cultivars. However, the continuous deployment of selected resistant varieties causes host selection pressures that drive Pt evolution and promote the incessant emergence of new virulent races, resulting in the demise of wheat-resistant cultivars after several years of planting. Intriguingly, diploid wheat accessions were found to confer haustorium formation-based resistance to leaf rust, which involves prehaustorial and posthaustorial resistance mechanisms. 

  • wheat
  • Puccinia triticina
  • leaf rust
  • resistance mechanisms
  • Lr genes
  • cloning
  • prehaustorial resistance
  • posthaustorial resistance
  • systemic acquired resistance

1. Introduction

Plants are continuously exposed to a wide range of pathogens and, accordingly, have evolved various defense mechanisms that facilitate early and vigorous pathogen detection and the mobilization of structural and biochemical defenses [1]. Thus, successful plant pathogen infection is more of a rarity than the rule [2]. Biotrophic plant fungal pathogens are the primary cause of most damaging plant diseases, primarily in cereal plants, which results in significant yield losses. Wheat leaf rust, caused by the basidiomycetous fungus Puccinia triticina Eriks. (Pt), is a macrocyclic foliar disease that continuously threatens wheat (Triticum aestivum L.) production in most wheat-growing regions and can cause significant yield losses over large geographical areas [3][4][5][6][7]. Leaf rust is among the most difficult wheat diseases to control because the pathogen has a high population diversity, the steady development of novel virulence profiles, and the pathogen can strongly adapt to new climate zones [8][9]. The combination of recent adaptations to warmer conditions and the constant rise in global temperature has led to an increase in the occurrence and severity of leaf rust epidemics. Given the vast size of the leaf rust population, it would be reasonable to predict that random mutations would occur with sufficient frequency, resulting in the emergence of new virulent races.
Wheat resistance to leaf rust can be divided into race-specific resistance and non-race-specific resistance based on genetic determinations, physiological features, and molecular mechanisms. Race-specific resistance is also called qualitative resistance or major gene resistance. It follows the gene-for-gene hypothesis [10] and is characterized by the presence of HR and induction of rapid cell death at the infection sites [3][11]. Non-race-specific resistance is also called adult plant resistance (APR), quantitative resistance, or slow-rusting resistance [12]. Histological observations revealed another two types of resistance mechanisms in wheat, namely prehaustorial and posthaustorial resistance [13][14][15]. Although many review articles have been published on the genetics of wheat resistance to rust [16][17][18][19][20][21][22][23][24], no review paper has been published that specifically focuses on haustoria formation-based resistance. Various studies have reported prehaustorial and posthaustorial resistance mechanisms against leaf rust in hexaploid wheat, but these studies have been mainly based on histopathological observations in which they were focusing on the fungal growth and development, specifically the haustorium [25]. Therefore, there is a need for the elucidation of the genetic background of haustorium formation-based resistance and how it is inherited. A recent study identified the genomic regions and candidate genes associated with prehaustorial resistance in T. monococcum [26]. 

2. Cloning and Characterization of Wheat Lr Genes

More than 100 leaf rust resistance (Lr) genes (~50% derived from wild progenitor and non-progenitor species) have been discovered, and only a few of these have been cloned so far [22][27]. The feasibility of cloning Lr genes or leaf rust resistance QTL (QLr) has been enhanced by advances in genomic sequencing and molecular biology techniques. Multiple strategies including classical map-based positional cloning or rapid gene-cloning approaches like MutRenSeq, AgRenSeq, MutChromSeq, and MutIsoSeq, as well as whole-genome sequencing, can be utilized to clone these genes [28][29]. So far, only eleven wheat Lr genes have been cloned (Table 1), either via classical map-based cloning, (Lr1 [30], Lr10 [31], Lr21 [32], Lr34 [33], Lr42 [34], and Lr67 [30][31][32][33][34][35]) or through rapid gene-cloning approaches such as MutRenSeq (Lr13) [36][37], TACCA (Lr22a) [38], MutChromSeq (Lr14a) [39], and MutIsoSeq (Lr9/Lr58) [40]. Most of the Lr genes that have been cloned, including Lr1, Lr10, Lr13, Lr21, Lr22a, and Lr42, are race-specific resistance genes that encode nucleotide-binding site leucine-rich repeat (NLR) proteins [30][31][32][34][37][38]. In addition to the NLR proteins, Lr14a is another race-specific resistance gene that encodes a membrane-localized protein with twelve ankyrin repeats and Ca2+-permeable non-selective cation channels [39]. Lr9/Lr58 is also a race-specific resistance gene which encodes a tandem kinase fusion protein [40]. Lr34 and Lr67 are known as slow-rusting genes or adult plant resistance genes, encoding a putative ATP- binding cassette (ABC) transporter and a hexose transporter, respectively [33][35].
Table 1. A summary of cloned Lr genes for leaf rust resistance.
Gene Chromosome Position R-Gene Product R-Gene Class Cloning Technique References
Lr1 5DL NLR ASR Map-based cloning [30]
Lr9/Lr58 6BL/2BL Tandem kinase–von Willebrand factor type-A domain fusion ASR MutIsoSeq [40]
Lr10 1AS NLR ASR Map-based cloning [31]
Lr13/Ne2 2BS NLR APR MutRenSeq [36][37]
Lr14a 7BL Ankyrin transmembrane domain protein ASR MutChromSeq [39]
Lr21 1DL NLR ASR Map-based cloning [32]
Lr22a 2DS NLR APR Map-based cloning and TACCA [38]
Lr34/Yr18/Sr57 7DS ATP-binding cassette transporter APR Map-based cloning [33]
Lr42 IDS NLR ASR BSR-Seq mapping [34]
Lr47 7AS NLR ASR Map-based cloning
EMTA approaches		 [41]
Lr67/Yr46/Sr55 4DL Anion transporter APR Map-based cloning [35]
NLR—Nucleotide-binding site leucine-rich repeat, ASR—all-stage resistance, APR—adult plant resistance.

3. Prehaustorial Resistance

Induced defense is prompted by the infection attempt of the respective pathogen. In rusts, one particularly common resistance feature is defective haustorium formation on non-host plant species and some resistant host species, termed prehaustorial or pre-cell-wall penetration resistance [42], and it is characterized by the expression of resistance prior to fungal penetration into the host. It was firstly described as reduced fungal penetration into the host during the interactions between rust fungi and non-hosts [43], and later, it was described in detail during the interactions between barley and leaf rust [14]. When partially resistant barley leaves were inoculated with leaf rust fungus Puccinia hordei, prehaustorial resistance was described as the inability to form a haustorium on the barley leaves. The inability to form haustorium results in a delayed progression of rust fungus growth (prolonged latency phase) and reduced or no spore production (no sporulation). Functional targets of prehaustorial resistance mechanisms are germ tubes and appressoria (ectophytic phase of pathogenesis), as well as substomatal vesicles and infection hyphae (early endophytic phase of the pathogenesis of rust fungi). This defense response typically leads to the formation of cell wall reinforcements, also called cell wall appositions or papillae [44][45]. Papillae were observed at the site of penetration and were shown not only to be involved in inhibiting pathogen penetration, but have also been implicated in repairing the cell wall subsequent to pathogen penetration attempts [46][47].
Mounting evidence has recently reported the participation of some wheat R genes in conferring prehaustorial resistance mechanisms that stop the development of rust fungi at the early endophytic and even ectophytic stages. It was reported that Lr1, Lr3a, Lr9, LrB, Lr19, Lr21, and Lr38 are involved in prehaustorial resistance to leaf rust [48]. The prehaustorial resistance level in T. monococcum seedlings was found to be higher than in Thatcher-Lr34 seedlings [46][49]. Prehaustorial resistance was associated with callose deposition and cellular lignification in the vicinity of the penetration site, and HR induction associated with the death of adjacent infected cells was also reported [51]. The prehaustorial resistance to wheat leaf rust discovered in the diploid wheat einkorn (T. monoccocum var. monococcum) accession PI272560 confers race-independent resistance against isolates that are virulent on accessions harboring resistance genes located on the A-genome of Triticum aestivum [52]. The establishment of prehaustorial resistance in accession PI272560 resulted in the abortion of fungal development during the formation of haustorial mother cells and the production of higher levels of H2O2 compared to the susceptible accession 36554 (T. boeoticum ssp. thaoudar var. reuteri) [52].
Some resistance mechanisms and transcriptome alterations were reported to be occurring in the background of PI272560 prehaustorial resistance because an increase in levels of phenolic substances and chitinase activity at the infection site, as well as pathogenesis-related genes, was observed at 24 h post-inoculation (hpi) compared to T. boeoticum accession (36554) [52]. It was recently found that a gene (TuG1812G0500002899) located on chromosome 5A, which encodes berberine bridge enzyme (BBE)-like Cyn d 4, was highly expressed at 8 hpi in PI272560 compared to the partially susceptible 36554 [26]. Serfling and colleagues reported that the BBE may instigate and trigger hypersensitive cell death [52], implying that it might be a critical enzyme for basal defense responses [53], but is also a key enzyme in non-host resistance [54][55]. As a progenitor of wheat, Triticum urartu is closely related to einkorn (T. monococcum), which often displays a high level of resistance to wheat leaf rust. Therefore, einkorn can be a useful resource for breeding pathogen-resistant wheat varieties in the future.
Only a few non-race-specific resistance genes are known, including Lr34, Lr46, and Lr67, which are only active during the adult phases of plant development [3]. The resistance imparted by Lr34 is distinguished by the absence of chlorosis and necrosis on flag leaves, as well as fewer and smaller uredinia, rather than a hypersensitive response [56]. During prehaustorial resistance, the formation of haustoria is frequently impeded prior to the development of fungal sporelings, which is caused by callose deposition at the site of cell wall penetration [57]. Similar to the quantitative resistance provided by Lr34, prehaustorial resistance is believed to confer resistance to Pt that is not specific to any particular race. However, it was observed that, in the majority of cases, prehaustorial resistance does not manifest as visible necrosis at the macroscopic level in T. monococcum accessions [46]. Lr67 has comparable traits to Lr34 in providing partial or slow-rusting, non-race-specific or broad-spectrum APR to leaf rust and stem rust. Lr67/Yr46/Sr55/Pm46/Ltn3 has been shown to provide partial resistance against leaf rust, stem rust (Sr55), stripe rust (Yr46), and powdery mildew (Pm46), and is associated with leaf tip necrosis (Ltn3) [58][59]. Since Lr34 and Lr67 confer non-race-specific resistance, which is not characterized by necrosis, it implies that these two genes impart prehaustorial resistance.

4. Posthaustorial Resistance

Posthaustorial resistance, also known as post-cell-wall penetration resistance, allows pathogen penetration into the host cells and the formation of haustorium by invaginating the host mesophyll cells [13][46]. Posthaustorial resistance is induced by the formation of at least one haustorium or, sometimes, the successful formation of pathogen colonies [51]. During posthaustorial resistance, the plant cell containing haustoria often dies, hence impeding the invasive growth and proliferation of the pathogen in adjacent cells, and this defense response is known as HR [13][60]. In general, race-specific hypersensitivity resistance is posthaustorial [46]. In host–pathogen interactions in which the host plant harbors race-specific resistance, the induction of HR occurs immediately after haustorium formation inside the host cells [43][46]. HR is also involved in the synthesis of secondary metabolites, the production of pathogenesis-related (PR) proteins, cell wall reinforcements, and in some cases, it is followed by ROS accumulation at the plasma membrane. Consequently, this results in an increased influx of Ca2+ levels, transcriptional reprogramming, and the activation of protein kinase cascades. Increased levels of H2O2 accumulation have been shown to trigger a signaling pathway that subsequently induces robust PCD [61]. During non-host interactions, the manifestation of posthaustorial resistance might occur at the position where haustoria formation occurs, and it may be enclosed in callose, leading to HR on the host cell. One notable distinction between gene-for-gene posthaustorial resistance and non-host posthaustorial resistance lies in their respective timing. Gene-for-gene posthaustorial resistance primarily manifests after the formation of haustoria, while non-host posthaustorial resistance initiates following pathogen penetration and persists throughout haustoria formation [62].

5. Systemic Acquired Resistance

Systemic acquired resistance (SAR) is a broad-spectrum resistance in plants that involves cellular processes such as the recognition of PAMPs or effectors, the transcriptional activation of battery of PR genes, MAPK signaling, and HR. The signal transduction pathway leading to SAR is principally regulated by NPR1 (non-expressor of PR genes), also called NIM1 (non-inducible immunity 1) [63][64][65][66][67][68]. SAR expression primarily depends on SA, a signaling molecule which triggers the expression of defense genes via NPR1 [69].NPR4 and its close homology NPR3 have functional redundancy in negatively regulating plant immunity [81]. Downstream of SA, two parallel signaling pathways have been hypothesized in recent research on NPR1, NPR3, and NPR4 [68]. On one hand, NPR3 and NPR4 suppress defense gene expression when SA levels are low, but when SA levels rise due to pathogen infection, NPR3 and NPR4 activities are reduced, and the transcriptional repression of SA-responsive genes is relaxed [68][82]. Pathogen-induced SA accumulation, on the other hand, enhances the transcriptional activation activity of NPR1 to further induce the expression of defense-related genes. Intricately woven together, they provide fine-tuned modulation of the defense response to varying levels of SA. A comprehensive review of the contribution of SA signaling via NPR1 and NPR3/4 to local and systemic defensive responses was also conducted by Liu and colleagues, and they established that most SA-triggered immune responses in plants require both types of SA receptors [83]. PR1, PR2, and PR5 are the PR genes that were demonstrated to be induced by SA, and these are also used as SA signaling markers [84].
The recognized function of the NPR1 protein in modulating SAR via the expression of PR genes has been documented in several plant species, such as Arabidopsis and rice, among others, under diverse biotic stress conditions [85]. Nine NPR1 homologues (TaNPR1) were identified in bread wheat [86][87], and it was recently postulated that NPR1 negatively regulates wheat resistance to stem rust infection by functioning at the Ta7ANPR1 locus via an NB-ARC-NPR1 fusion protein [87]. However, the role of the wheat NPR1 homologues in wheat defense responses against leaf rust remains a mystery. A potentially more sophisticated host might include using TaNPR1 as a decoy in the detection, while also developing an alternate mechanism to circumvent TaNPR1 in instances when the integrity of the NPR1 component is disrupted by pathogens [87]. The comprehensive understanding of the functions of wheat NPR1 homologues in wheat resistance to leaf rust may facilitate the development of approaches to alter the interactions between wheat and Pt through the modification of the expression of the respective genes, utilizing transgenic or genome-editing technologies like CRISPR/Cas9 to impart broad-spectrum resistance in wheat [88].

6. Future Prospects and Limitations 

Clearly, the effective management of leaf rust necessitates a basic understanding of the diversity and virulence profiles of the pathogen populations acquired using a race survey analysis approach. These surveys aid in predicting the occurrence of epidemics and provide valuable insights that may be effectively used by breeders and agronomists for integrated disease management strategies. The use of einkorn wheat as a genetic resource in wheat breeding has been documented. However, the scarcity of comprehensive genetic and genomic datasets pertaining to einkorn wheat, as well as its genome organization, is a significant challenge in the field of wheat breeding, given the paramount significance of einkorn wheat in this domain. Recently an einkorn genome database was unveiled, and it ushers in an interface for the research community that focuses on cereals to enhance their breeding programs by using comparative genomic and applied genetics. While T. monococcum is not the immediate progenitor of the A-genome in bread wheat, it exhibits significant homology to the A-genome seen in present cultivated hexaploid and tetraploid wheat, and gene transfers between bread wheat and T. monococcum are indeed possible. Therefore, the utilization of diploid wheat accessions conferring high prehaustorial resistance to leaf rust may broaden the durable resistance pool against leaf rust, and may also be used to replace the commonly used race-specific and single-gene resistance.

Understanding the sources and distribution patterns of leaf rust resistance genes has significant importance in the development of novel wheat cultivars with durable resistance. The wild relatives of wheat continue to be very significant sources for the identification of novel genetic loci that contain the Lr/QLr genes. The identification of novel quantitative trait loci associated with various Pt races can aid future wheat-breeding programs through the recombination of different loci for durable resistance to leaf rust races. Therefore, there is still a need to explore resistant germplasm, especially introgression lines derived from wheat wild relatives. Further investigation is required to ascertain the optimal approaches for incorporating the rapidly advancing knowledge from several disciplines into effective regional breeding initiatives. The wild relatives of wheat provide a greater reservoir of R genes because they have not undergone the genetic bottleneck feature of domestication.

This entry is adapted from the peer-reviewed paper 10.3390/plants12233996

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