microRNA‐encoded peptides inhibit seed germination of the root parasitic plant Orobanche cumana

Abstract

Societal Impact StatementThe root parasitic plant Orobanche cumana (sunflower broomrape) is one of the major pests of sunflower crops. Despite intense efforts to develop effective agricultural practices and breeding programs, selective control of broomrapes is still rare and ineffective in terms of sustainability. It is thus essential to develop new specific control methods against those pests. miRNA‐encoded peptides (miPEPs) are a new class of peptides regulating the expression of miRNAs and their corresponding target genes. This study demonstrates that certain miPEPs strongly inhibit the germination of broomrape seeds by regulating their miR gene, making them good candidates for use as biocontrol agents against this pathogen.Summary Root parasitic plants of the Orobanchaceae family are a constant and growing threat to agriculture worldwide. Among them, the parasitic weed Orobanche cumana, the sunflower broomrape, causes significant losses to sunflower production in European‐Asian and North African countries. Despite the use of several conventional control methods against this pathogen, none has proved effective or durable, underlining the need to develop innovative strategies. miRNA‐encoded peptides (miPEPs) are regulatory peptides stimulating the expression of their own primary transcript of miRNA, and plant watering with those molecules leads to down‐regulating specifically miRNA target genes and altering plant physiology. Through seed germination assays and qRT‐PCR analysis, we investigated the impact of exogenous treatments of synthetic miPEPs on broomrape seed germination. First, we report that the conserved miRNA repertoire of O. cumana consists of 39 members. Thirty‐nine miPEPs were designed, synthetized, and assayed, 11 of which strongly inhibited O. cumana seed germination. Interestingly, miPEP319a showed the strongest inhibiting effect while miPEP319b did not. Three out of the four corresponding miR319 target genes showed upregulation after treatment with a germination stimulant, which was impaired by treatment with miPEP319a. This downregulation of expression is associated with an increase in the expression of the corresponding pri‐miR319a. We reveal thus that the use of miPEPs can increase our knowledge of key molecular mechanisms underlying a complex parasite interaction and should provide a new phytosanitary method to control broomrape parasitism with highly specific and biodegradable natural substances.