BRing on the fight! Brassinosteroid-related transcription factors modulate resistance to fungi attack in wheat

Brassinosteroids (BRs) are a class of plant-specific polyhydroxylated steroid hormones that function as master regulators of plant development and are involved in a plethora of processes, including seed germination, growth, tissue differentiation, flowering, and senescence. BRs are also recognized as important mediators of plant responses to external stimuli, including light, temperature, water availability, and salinity (Wang et al., 2012; Ahammed et al., 2020), and are now gaining attention for their broad involvement in the regulation of defense responses against pest and pathogen attack (Campos et al., 2009; Lozano-Durán and Zipfel, 2015). In this sense, numerous genetic components of the BR signaling pathway have been recognized for their key role in triggering the plant immune system. For instance, the BRASSINOSTEROID INSENSITIVE 1 (BRI1)-ASSOCIATED RECEPTOR KINASE1 (BAK1), a protein kinase that works as a coreceptor of the BR receptor BRI, is recognized as one of the central regulators of innate immunity in plants (Heese et al., 2007). BRI and BAK1 regulate the activity of the BRI1-EMS suppressor (BES)/brassinazole-resistance (BZR) family of transcription factors, whose participation in defense responses is described but largely uncomprehended at the molecular level (Li et al., 2020). Unfortunately, this knowledge gap hinders our capacity to fully understand how BRs regulate responses to biotic stresses and to develop cultivars with increased resistance to pest and pathogen attack.

In this issue of Plant Physiology, Bai et al. (2021) shed some light on this topic by uncovering how the wheat (Triticum aestivum) BES/BZR-type transcription factor TaBZR2 mediates resistance to wheat stripe rust fungus (Puccinia striiformis f. sp. Tritici, or simply Pst), one of the most impactful threats to wheat production worldwide. The authors began by analyzing transcriptome data of wheat plants inoculated with Pst, where they found TaBZR2 was the only wheat BZR whose expression was upregulated during fungal infection (when compared to noninoculated plants). To explore the involvement of TaBZR2 in immunity, the authors then evaluated TaBZR2 expression in wheat seedlings treated with two defense elicitors, flg22 and Pst322. TaBZR2 transcript levels were quickly (0.5 h post-treatment) and strongly (up to 9-fold increase) upregulated when seedlings are treated with these elicitors, suggesting that this transcription factor is involved in wheat defense responses against pathogen attack.

To evaluate the role of TaBZR2 in defense against Pst, Bai et al. (2021) developed transgenic wheat plants overexpressing TaBZR2 (TaBZR2-OE), which were then subjected to resistance assays upon infection with nine different Pst races. Compared to infected wild-type (WT) plants TaBZR2-OE lines plants showed enhanced resistance against five Pst races (including three of the prevalent Pst races in China) as demonstrated by lower fungal biomass as well as the number of uredia (spore-producing bodies) present on leaves. Histological examination also demonstrated that the length of hyphae, number of haustorial mother cells, and infection areas were smaller in TaBZR2-OE when compared to WT plants 120 h post-infection. Moreover, TaBZR2-OE lines also accumulated more hydrogen peroxide (H₂O₂), a molecule that functions as a defensive trait and immunity secondary messenger in plants (Orozco-Cárdenas et al., 2001), around the infection sites. Taken together, these data indicate that TaBZR2 is involved with broad-spectrum resistance to Pst in wheat. This hypothesis was confirmed by suppression of TaBZR2 expression in wheat via RNAi-mediated knockdown, which led to compromised resistance of wheat to infection by multiple races of Pst when compared to WT plants.

To gain insight into the molecular mechanisms regulated by TaBZR2 to confer fungi disease resistance, Bai et al. (2021) performed transcriptome analysis of WT and TaBZR2-OE plants challenged by Pst infection. Analysis of differentially expressed genes between these two genotypes indicated an enrichment of transcripts involved with “chitin binding” and “chitinase activity” in TaBZR2-OE plants after pathogen attack. As chitinases represent one of the most prominent defense responses against fungi infection and one of the most relevant mechanisms sought for increased crop resistance against pathogen attack (Kumar et al., 2018), the authors focused their attention on TaCht20.2, a chitinase gene whose expression increased ∼20-fold in TaBZR2-OE plants infected with Pst when compared to noninoculated WT plants. Using electrophoretic mobility shift assays and luciferase reporter gene analysis, Bai et al. (2021) demonstrated that TaBZR2 is capable of binding to cis-elements (E-box) present in the promoter of TaCht20.2 to drive its expression. The role of TaCht20.2 in wheat resistance to Pst infection was demonstrated by producing transgenic plants where the expression of this gene was ablated by virus-induced gene silencing (TaCht20.2-knockdown). Fungal biomass and infection area per infection site increased in TaCht20.2-knockdown plants infected with Pst strains when compared to WT infected plants. Decreased H₂O₂ accumulation after Pst infection in the knockdown plants also indicated that TaCht20.2 is an important player in wheat resistance to Pst.

Pest and pathogen attack is one of the main causes of economic losses and reduced food security worldwide, and it is estimated that >20% of wheat production is lost because of biotic stress (Savary et al., 2019). Work by Bai et al. (2021) uncovers a molecular mechanism associated with resistance against Pst, one of the most troublesome pathogens of wheat. Although the potential of manipulating TaCht20.2 expression outside the laboratory environment and whether other chitinases are involved in defense response against this pathogen remains unknown, their proposed model (Figure 1) provides a useful resource that may already aid geneticists to produce more resistant wheat cultivars.

Figure 1.

TaBZR2 is a regulator of wheat defense responses against P. striiformis f. sp. Tritici (Pst) infection. In this issue of Plant Physiology, Bai et al. (2021) demonstrate that Pst infection leads to upregulation of the BR-related transcription factor TaBZR2, which can bind the promoter of TaCht20.2 to upregulate its expression. TaCht20.2 is a chitinase with activity that leads to increased defense against Pst infection.