Cyclophilin 20-3 coordinates plant root hair growth and resistance against parasitic nematodes

Plant parasitic nematodes (PPN) are a major threat to agriculturally important crops, resulting in substantial yield losses and economic repercussions. However, the underlying modes of plant-PPN interactions remain largely elusive. Here, we describe a critical role of cyclophilin (CYP)20-3, a plastid dual enzyme [i.e., peptidyl-prolyl isomerase (PPIase) and reductase) in plant basal resistance against PPN attacks. Originally, in order to define a present working model of whether plant roots deploy hypersensitive response (HR) to restrict PPN infections, we co-imaged the 'real-time' interactions of a proposed HR system, cotton LONREN-1 vs. Rotylenchulus reniformis. The root imaginings, however, revealed no clear HR pattern, instead underpinning a negative relationship between PPN populations and extended root hair growth. The latter was then identified to couple with the spatial expression of PPIases, including homologs of CYP20-3, a known receptor of 12-oxophytodienoic acid (OPDA) signal. To elaborate these findings further, we employed a reverse generic approach using a model plant Arabidopsis, and illuminated that knockout cyp20-3 mutants i) abnormalize root hair formations and ii) enhance susceptibility to PPN, Meloidogyne hapla, challenges. Nevertheless, M. hapla infections did not induce OPDA synthesis and signaling marker gene expressions in Arabidopsis roots. In parallel, transgenic Arabidopsis plants overexpressing mutant CYP20-3s defective OPDA-binding/signaling (H140Q) or PPIase (F74L) could still improve plant PPN defenses, whereas the overexpression of CYP20-3C129S (-reductase) demonstrated WT-level galling formations. Thus, we conclude that OPDA-independent CYP20-3-reductase signaling plays a key role in the plant defense metabolic pathway, fortifying protective barriers and conferring innate resistance against PPN attacks.