The AtCRK5 Protein Kinase Is Required to Maintain the ROS NO Balance Affecting the PIN2-Mediated Root Gravitropic Response in Arabidopsis

Abstract

The Arabidopsis AtCRK5 protein kinase is involved in the establishment of the proper auxin gradient in many developmental processes. Among others, the Atcrk5-1 mutant was reported to exhibit a delayed gravitropic response via compromised PIN2-mediated auxin transport at the root tip. Here, we report that this phenotype correlates with lower superoxide anion (O2•−) and hydrogen peroxide (H2O2) levels but a higher nitric oxide (NO) content in the mutant root tips in comparison to the wild type (AtCol-0). The oxidative stress inducer paraquat (PQ) triggering formation of O2•− (and consequently, H2O2) was able to rescue the gravitropic response of Atcrk5-1 roots. The direct application of H2O2 had the same effect. Under gravistimulation, correct auxin distribution was restored (at least partially) by PQ or H2O2 treatment in the mutant root tips. In agreement, the redistribution of the PIN2 auxin efflux carrier was similar in the gravistimulated PQ-treated mutant and untreated wild type roots. It was also found that PQ-treatment decreased the endogenous NO level at the root tip to normal levels. Furthermore, the mutant phenotype could be reverted by direct manipulation of the endogenous NO level using an NO scavenger (cPTIO). The potential involvement of AtCRK5 protein kinase in the control of auxin-ROS-NO-PIN2-auxin regulatory loop is discussed.

Reactive Oxygen Species in Plants: From Source to Sink

“…The production of ROS during stress (abiotic) results in changes in auxin gradients that, in turn, reduce auxin-induced signaling. Auxins can also induce ROS production and help in maintaining ROS homeostasis, exhibiting an association between oxidative stress and auxin signaling [ 35 ]. Auxins also play a role in the activation of RAC/ROP (Rho-GTPase), which further interact with NADPH oxidases that cause apoplastic production of ROS.…”

Molecular Evolution of Calcium Signaling and Transport in Plant Adaptation to Abiotic Stress

“…Thus, the Ca 2+ -dependent manner of CRKs is binding with CaMs rather than being directly regulated by Ca 2+ [118]. For example, one of the functions of CRKs is the positive regulation of root growth and gravitropism via establishment of the proper auxin gradient and modulation of polar auxin transport (PAT) proteins [119][120][121]. In short, CDPK subfamilies are vital regulatory nodes in Ca 2+ signaling pathways and abiotic stress in plants.…”

The ROP2 GTPase Participates in Nitric Oxide (NO)-Induced Root Shortening in Arabidopsis

“…PIN1 transcription was reported to be rather sensitive to conditions affecting auxin transport and distribution [ 52 ]. Furthermore, there are experimental data showing that endogenous as well as exogenous NO influences the auxin transport pattern in the Arabidopsis root meristem in a PIN2 stability- and distribution-dependent manner [ 53 , 54 ]. Therefore, it is also possible that the NO-induced and PIN2-dependent auxin decrease in the root meristem feeds back to reduce PIN1 as well as PIN2 transcription.…”

“…Interestingly, however, NO-mediated S-nitrosation of the auxin receptor TRANSPORT INHIBITOR RESPONSE 1 (TIR1) had a positive effect on auxin signaling [ 42 ]. Furthermore, auxin is known to regulate the endogenous NO levels [ 42 , 53 , 54 ]. Therefore, auxin and NO can be part of complex regulatory loops required to maintain root meristem functions [ 54 ].…”