Impact of Plant Peptides on Symbiotic Nodule Development and Functioning

Abstract

Ribosomally synthesized peptides have wide ranges of functions in plants being, for example, signal molecules, transporters, alkaloids, or antimicrobial agents. Legumes are an unprecedented rich source of peptides, which are used to control the symbiosis of these plants with the nitrogen-fixing Rhizobium bacteria. Here, we discuss the function and the evolution of these peptides playing an important role in the formation or functioning of the symbiotic organs, the root nodules. We distinguish peptides that can be either cell-autonomous or secreted short-range or long-range signals, carrying messages in or between plant cells or that can act as effectors interacting with the symbiotic bacteria. Peptides are further classified according to the stage of the symbiotic process where they act. Several peptide classes, including RALF, DLV, ENOD40, and others, control Rhizobium infection and the initiation of cell divisions and the formation of nodule primordia. CLE and CEP peptides are implicated in systemic and local control of nodule initiation during autoregulation of nodulation and in response to the nutritional demands of the plant. Still other peptides act at later stages of the symbiosis. The PSK peptide is thought to be involved in the suppression of immunity in nodules and the nodule-specific cysteine-rich, GRP, and SNARP (LEED..PEED) peptide families are essential in the functioning of the nitrogen fixing root nodules. The NCRs and possibly also the GRP and SNARPs are targeted to the endosymbionts and play essential roles in the terminal differentiation of these bacteria.

Plant transcriptome analysis reveals specific molecular interactions between alfalfa and its rhizobial symbionts below the species level

“…This eventually leads to the formation of symbiosomes wherein atmospheric nitrogen is converted into ammonium [2,3]. The terminal bacteroid differentiation process is governed by nodule-specific peptides such as small nodulin acidic RNA binding proteins (SNARPs), nodule-specific cysteine-rich peptides (NCRs) and glycine-rich proteins (GRPs) [4,5]. They are thus required for the establishment of highly efficient nitrogenfixation symbiotic systems.…”

Insights into the evolution of symbiosis gene copy number and distribution from a chromosome-scale Lotus japonicus Gifu genome sequence

“…It should be noted that many of the transcripts classified as long non-coding RNAs in the Medicago study 41 in fact encode peptides, most notably the large family of nodule cysteine-rich (NCR) peptides. The NCR peptides are characteristic of the Inverted Repeat Lacking Clade (IRLC) legume lineage and thus not found in Lotus50 . The same appears to be the case for the other transcripts in the non-coding class, indicating that non-coding and peptideencoding genes have evolved rapidly and are not generally required for legume-rhizobium symbiosis across determinate and indeterminate nodulators.…”

MtSSPdb: The Medicago truncatula Small Secreted Peptide Database

“…The co-expressing SSPs were predominantly NCR, leginsulin, and plant defensin genes ( Figure 9C). NCR genes in particular encode nodule-specific SSPs with roles in development and maintenance of rhizobia within symbiotic nodules in Medicago truncatula (Kereszt et al, 2018). Thus, the expression patterns discerned from MtSSPdb may indicate a role in nodulation for CAPE16, but further experiments should be conducted to validate these findings.…”

“…SSPs have emerged as an important class of regulatory molecules involved in plant growth, development, plant-microbe interactions, and stress tolerance (Czyzewicz et al, 2013, Nakaminami et al, 2018, Takahashi et al, 2018. This is of particular significance for legumes, since recent discoveries show that SSPs regulate symbiotic root nodulation (Djordjevic et al, 2015, Nishida et al, 2018, Kereszt et al, 2018, and root development (Araya et al, 2016, Patel et al, 2018. SSPs are also involved in reproductive development, embryogenesis, and pathogen interaction, among many other plant processes (Breiden andSimon, 2016, Matsubayashi, 2014).…”