Danger-Associated Peptides Interact with PIN-Dependent Local Auxin Distribution to Inhibit Root Growth in Arabidopsis

Abstract

Plant elicitor peptides (Peps) are damage/danger-associated molecular patterns that are perceived by the receptor-like kinases, PEPR1 and PEPR2, to enhance innate immunity and to inhibit root growth in Arabidopsis (Arabidopsis thaliana). Here, we show that Arabidopsis Pep1 inhibits root growth in a PEPR2-dependent manner, which is accompanied by swelling epidermal and cortex cells and root hair formation in the transition zone (TZ). These Pep1-induced changes were mimicked by exogenous auxin application and were suppressed in the auxin perception mutants transport inhibitor response1 (tir1) and tir1 afb1 afb2. Pep1-induced auxin accumulation in the TZ region preceded cell expansion in roots. Because local auxin distribution depends on PIN-type auxin transporters, we examined Pep1-PEPR-induced root growth inhibition in several pin mutants and found that pin2 was highly sensitive but pin3 was less sensitive to Pep1. The pin2 pin3 double mutant was as sensitive to Pep1 treatment as wild-type plants. Pep1 reduced the abundance of PIN2 in the plasma membrane through activating endocytosis while increasing PIN3 expression in the TZ, leading to changes in local auxin distribution and inhibiting root growth. These results suggest that Pep-PEPR signaling undergoes crosstalk with auxin accumulation to control cell expansion and differentiation in roots during immune responses.

Danger-Associated Peptide Regulates Root Growth by Promoting Protons Extrusion in an AHA2-Dependent Manner in Arabidopsis

“…To investigate whether Pep1 interacts with pH signaling to regulate the root growth, we examined the effects of 100 nM Pep1 in the plant growth medium with different pH (4.5 to 8.0) on the growth of wild-type (WT) seedlings. Pep1 treatment induced a significant root growth inhibition under normal pH (5.8) condition ( Figure 1A,B), in agreement with previous results [15]. Interestingly, we found that Pep1's effect on root growth was dependent on the pH changes, as decreasing of medium pH (4.5-5.8) further aggravated the Pep1-induced root growth inhibition, however, increasing of medium pH into faintly acid (pH 6.4), neutral (pH 7.2), or alkali (pH 8.0) condition significantly alleviated the Pep1 effect on root growth ( Figure 1A,B).…”

“…In the process of revealing the role of Pep-PEPR in plants, we found that binding of Pep1 to PEPR2 induced a strong root growth inhibition, accompanied by swelling epidermal and cortical cells in root transition zone (TZ) [15]. In this study, we revealed that Pep1 treatment inhibited the root growth by activating the PM H + -ATPase to extrude the protons into apoplast, which induced an overly acidic environment in apoplast to inhibit root growth.…”

“…The application of PAMPs (such as flg22 and efl18) or DAMPs (such as Peps) could activate root immune response (including elevated cytosolic Ca2+ levels, reactive oxygen species (ROS) bursts, callose deposition, and defense-related gene expression, etc.) and induce the root growth inhibition [14][15][16]19]. Our previous results indicated that the Pep1-PEPRs system triggered a strong root growth inhibition by intersecting with auxin and ROS signaling pathways, both of which were activated by Pep1 treatment that in turn inhibits root growth [15,16].…”

“…The root growth is affected by pH changes. Our previous results indicated that Pep1 triggered a strong root growth inhibition accompanied by swelling epidermal and cortex cells in root apex and decreasing root meristem size [15]. To investigate whether Pep1 interacts with pH signaling to regulate the root growth, we examined the effects of 100 nM Pep1 in the plant growth medium with different pH (4.5 to 8.0) on the growth of wild-type (WT) seedlings.…”

“…Among the two receptors, PEPR1 is documented 2 of 15 as the predominant receptor for eight Peps in regulating the leaf immunity [6,13]. However, PEPR2 primarily detects Pep1 and Pep2 ligands and functions in root to regulate the root immunity and growth [14][15][16].…”