Loss of function of a DMR6 ortholog in tomato confers broad-spectrum disease resistance

Abstract

Plant diseases are among the major causes of crop yield losses around the world. To confer disease resistance, conventional breeding relies on the deployment of single resistance (R) genes. However, this strategy has been easily overcome by constantly evolving pathogens. Disabling susceptibility (S) genes is a promising alternative to R genes in breeding programs, as it usually offers durable and broad-spectrum disease resistance. In Arabidopsis, the S gene DMR6 (AtDMR6) encodes an enzyme identified as a susceptibility factor to bacterial and oomycete pathogens. Here, we present a model-to-crop translational work in which we characterize two AtDMR6 orthologs in tomato, SlDMR6-1 and SlDMR6-2. We show that SlDMR6-1, but not SlDMR6-2, is up-regulated by pathogen infection. In agreement, Sldmr6-1 mutants display enhanced resistance against different classes of pathogens, such as bacteria, oomycete, and fungi. Notably, disease resistance correlates with increased salicylic acid (SA) levels and transcriptional activation of immune responses. Furthermore, we demonstrate that SlDMR6-1 and SlDMR6-2 display SA-5 hydroxylase activity, thus contributing to the elucidation of the enzymatic function of DMR6. We then propose that SlDMR6 duplication in tomato resulted in subsequent subfunctionalization, in which SlDMR6-2 specialized in balancing SA levels in flowers/fruits, while SlDMR6-1 conserved the ability to fine-tune SA levels during pathogen infection of the plant vegetative tissues. Overall, this work not only corroborates a mechanism underlying SA homeostasis in plants, but also presents a promising strategy for engineering broad-spectrum and durable disease resistance in crops.

Roles of the 2-Oxoglutarate-Dependent Dioxygenase Superfamily in the Flavonoid Pathway: A Review of the Functional Diversity of F3H, FNS I, FLS, and LDOX/ANS

“…Catalyzing the C-5 hydroxylation of SA is a new function of FNS I, which has been verified in Arabidopsis and tomato [53,67]. The traditional physiological function of FNS I in most angiosperms is proposed to be lost and replaced by that of CYP FNS II, though the activity of FNS I in rice, maize, and Arabidopsis were studied [13,45,[68][69][70].…”

“…SlDMR6-1 and SlDMR6-2 display SA-5 hydroxylase activity, converting SA into 2, 5-DHBA in vitro, while in tomato, SlDMR6-1, but not SlDMR6-2, was upregulated by pathogen infection, and a Sldmr6-1 mutant displayed enhanced resistance against differ-ent classes of pathogens. However, the purified SlDMR6-1 and SlDMR6-2 proteins only displayed S5H activity in vitro and failed to catalyze the conversion of naringenin [67].…”

“…Therefore, AtDMR6 is known as an FNSI homolog, also called S5H. Recently, two orthologs of AtDMR6 were characterized in tomato and were named SlDMR6-1 and SlDMR6-2 [67]. SlDMR6-1 and SlDMR6-2 display SA-5 hydroxylase activity, converting SA into 2, 5-DHBA in vitro, while in tomato, SlDMR6-1, but not SlDMR6-2, was upregulated by pathogen infection, and a Sldmr6-1 mutant displayed enhanced resistance against differ-ent classes of pathogens.…”

“…Only a few FNSs I from non-Apiaceae species including rice, maize, and A. thaliana were studied in detail [13,45]. However, in this branch, both AtDMR6 and SlDMR6 displayed SA-5 hydroxylase activity, with no FNS activity [67]. In addition, the FNS I branch is more closely related to S3Hs, which also form a distinct subgroup.…”

Tal2c Activates the Expression of OsF3H04g to Promote Infection as a Redundant TALE of Tal2b in Xanthomonas oryzae pv. oryzicola

“…For instance, gene editing of StDMR6-1 in potato, ObDMR6 in sweet basil and MusaDMR6 in banana was found to specifically enhance resistance to late blight [27], downy mildew [28] and banana Xanthomonas wilt [29]. Moreover, gene editing of SlDMR6-1 increases broad-spectrum disease resistance to bacteria, oomycetes and fungi in tomato [30]. In rice, the flavanone 3-hydroxylase (F3H) gene OsF3H 03g is the target of Tal2b and Tal9b from Xoc and Xoo, respectively [13,18], which is involved in positively regulating resistance to brown planthoppers by accumulating flavonoid content [31], as well as negatively regulating resistance to BB, BLS and sheath blight along with a reduction of SA [4].…”