ROS production by localized SCHENGEN receptor module drives lignification at subcellular precision

Abstract

26Production of reactive-oxygen species (ROS) by NADPH oxidases (NOXs) impacts many 27 processes in animals and plants and many plant receptor pathways involve rapid, NOX-dependent 28 increases of ROS. Yet, their general reactivity has made it challenging to pinpoint the precise role 29 and direct cellular targets of ROS. A well-understood ROS target in plants are lignin peroxidases 30 in the cell wall. Lignin can be deposited with exquisite spatial control, but the underlying 31 mechanisms have remained elusive. Here we establish a full kinase signaling relay that exerts 32 direct, spatial control over ROS production and lignification within the cell wall. We show that 33 polar localization of a single kinase component is crucial for pathway function. Our data indicates 34 that an intersection of more broadly localized components allows for micrometer-scale precision 35 of lignification and that this system is triggered through initiation of ROS production as a critical 36 peroxidase co-substrate. 37 As in animals, NADPH oxidase-produced ROS in plants is important for a multitude of 38 processes and the number of NADPH oxidase genes (10 in Arabidopsis, called RESPIRATORY 39 BURST OXIDASE HOMOLOGs, RBOHs, A-J) suggests a high complexity of regulation of ROS 40 production in plants. Among its many roles, ROS-dependent regulation of plant cell wall structure and 41 function is considered to be among its most critical 1 . The cell wall is the nano-structured, sugar-based, 42 2 pressure-resisting extracellular matrix of plants and NOXs are thought to be the predominant ROS 43 source in this compartment (also termed apoplast) 1 . 44A staggering number of kinases have been shown to regulate plant NOXs and the activation 45 mechanism of NOX-dependent ROS production is well established, especially in response to microbial 46 pattern-recognition by immune receptors 2 . However, the specific role and direct molecular targets of 47 ROS during microbial pattern-recognition have remained elusive 3 . The same applies for the central 48 role of ROS in tip growing cells, such as root hairs or pollen tubes, where ROS is thought to be part of 49 an intricate oscillation of cell wall stiffening and loosening, aimed at allowing cell wall expansion 50 without catastrophic collapse 4,5 . In this case, ROS is proposed to be important for counteracting cell 51 wall loosening pH decreases, but it is again unclear what direct targets of ROS would mediate cell wall 52 stiffening. Cell wall lignification by apoplastic peroxidases, can therefore be considered as the most 53 well-established role of ROS, where the peroxidases themselves are the direct "ROS targets", using it 54 as a co-substrate for the oxidation of mono-lignols 6,7 . In the case of lignification, however, a 55 molecularly-defined signaling pathway that induces ROS production during lignification has not been 56 defined. A few years ago, our group identified a specific NADPH oxidase, RBOHF, to be required for 57 the localized formation of lignin in the root end...

Flavonols modulate lateral root emergence by scavenging reactive oxygen species in Arabidopsis thaliana

“…A study identifying proteins that contain an oxidative modification in Arabidopsis found that 4% of detected proteins were enriched in cell wall proteins ( 81 ). For instance, RBOHF has been shown to regulate lignification of plant cell walls ( 82 ). Hydrogen peroxide has been implicated in strengthening of the cell wall through cross-linking of cell wall polymers ( 83 ).…”

Flavonols modulate lateral root emergence by scavenging reactive oxygen species inArabidopsis thaliana

“…A study identifying proteins that contain an oxidative modification in Arabidopsis found 4% of detected proteins were enriched in cell wall proteins (72). For instance, RBOHF has been shown to be regulate lignification of plant cell walls (73). Hydrogen peroxide has been implicated in strengthening of the cell wall through crosslinking of cell wall polymers (74).…”

Uclacyanin proteins are required for lignified nanodomain formation within Casparian strips

“…Furthermore, we observed ectopic 191 lignification on the cortical side of the endodermis on a few occasions in the ucc1 mutants, 192 and at a higher frequency in the double mutant ucc1.2 ucc2.1 ( Figure 4A-B, Supplementary 193 figure 4). This is a typical phenotype, along with increased suberin deposition, that is due to 194 the SGN3-dependent compensatory mechanism observed in most mutants with defective CS 195 9 [1,2,14, 18,33]. However, the ectopic lignification and enhanced suberization are observed to 196 a lesser degree in ucc1.2 ucc2.1 in comparison with other CS mutants such as casp1 casp3 197 and esb1 mutants ( Figure 1D In conclusion, this study reveals the first loss-of-function phenotype for members of the 204 plant-specific blue copper protein family of phytocyanins.…”