Next Article in Journal
Volatile Compounds in Norway Spruce (Picea abies) Significantly Vary with Season
Previous Article in Journal
Characterizing Root Morphological Responses to Exogenous Tryptophan in Soybean (Glycine max) Seedlings Using a Scanner-Based Rhizotron System
 
 
Search for Articles:
Title / Keyword
Author / Affiliation / Email
Journal
Article Type
 
 
Advanced Search
 
Section
Special Issue
Volume
Issue
Number
Page
 
Journals
Plants
Volume 12
Issue 1
10.3390/plants12010187
plants-logo
Submit to this Journal Review for this Journal Propose a Special Issue
► Article Menu

Article Menu

share Share announcement Help format_quote Cite question_answer Discuss in SciProfiles thumb_up
...
Endorse textsms
...
Comment
first_page
settings
Order Article Reprints
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:
Background:
Review

Plants Recruit Peptides and Micro RNAs to Regulate Nutrient Acquisition from Soil and Symbiosis

by
Marios I. Valmas
1,
Moritz Sexauer
2,
Katharina Markmann
2 and
Daniela Tsikou
1,*
1
Department of Biochemistry and Biotechnology, University of Thessaly, Biopolis, 41500 Larissa, Greece
2
Julius-von-Sachs-Institute for Biosciences, Würzburg University, Julius-von-Sachs-Platz 3, 97082 Würzburg, Germany
*
Author to whom correspondence should be addressed.
Plants 2023, 12(1), 187; https://doi.org/10.3390/plants12010187
Submission received: 6 December 2022 / Revised: 24 December 2022 / Accepted: 27 December 2022 / Published: 2 January 2023
(This article belongs to the Special Issue Transcriptomic and Proteomic Response of Plants to Nutritional Deficiency)
Browse Figure
Versions Notes

Abstract

:
Plants engage in symbiotic relationships with soil microorganisms to overcome nutrient limitations in their environment. Among the best studied endosymbiotic interactions in plants are those with arbuscular mycorrhizal (AM) fungi and N-fixing bacteria called rhizobia. The mechanisms regulating plant nutrient homeostasis and acquisition involve small mobile molecules such as peptides and micro RNAs (miRNAs). A large number of CLE (CLAVATA3/EMBRYO SURROUNDING REGION-RELATED) and CEP (C-TERMINALLY ENCODED PEPTIDE) peptide hormones as well as certain miRNAs have been reported to differentially respond to the availability of essential nutrients such as nitrogen (N) and phosphorus (P). Interestingly, a partially overlapping pool of these molecules is involved in plant responses to root colonization by rhizobia and AM fungi, as well as mineral nutrition. The crosstalk between root endosymbiosis and nutrient availability has been subject of intense investigations, and new insights in locally or systemically mobile molecules in nutrient- as well as symbiosis-related signaling continue to arise. Focusing on the key roles of peptides and miRNAs, we review the mechanisms that shape plant responses to nutrient limitation and regulate the establishment of symbiotic associations with beneficial soil microorganisms.

1. Introduction

Plant growth and development depend on the acquisition of a number of mineral nutrients from the soil. Essential nutrients such as nitrogen (N) and phosphorus (P) have key roles in agriculture, as their limitation is considered a frequent cause of reduced crop productivity. Most land plants meet nutrient limitation in terrestrial environments by associating with beneficial microorganisms. Arbuscular mycorrhizal (AM) associations with fungi and N-fixing root nodulation of legume plants with rhizobial bacteria improve the acquisition of mineral elements, such as P and N. Microbial inoculants are increasingly used as biofertilizers, and tested for their potential to replace cost-intensive and environmentally harmful synthetic P and N fertilizers in agricultural settings.
This review discusses the role of peptides and micro RNAs (miRNAs) in mediating the plant responses to N and P availability and the establishment and control of symbiotic relationships improving N and P acquisition.

2. Plants Associate with Soil Microorganisms to Access Essential Nutrients

Root nodule symbiosis is an endosymbiotic association formed between legumes and rhizobial bacteria. Under symbiotic conditions, the latter fix aerial N2 through the enzyme nitrogenase, converting it to ammonia (NH3) (reviewed in [1]). Upon release to the peribacteroid space that separates symbiotic bacteria from the infected host cell, NH3 is converted to ammonium (NH4+), which is then released to the plant cytosol [2]. NH4+ transporters have been characterized in legumes, as in soybean (Glycine max) [3] and Lotus japonicus [4]. In return for fixed N, plants provide rhizobia with branched amino acids, sugars and micronutrients essential for bacterial development. Besides that, dicarboxylic acids, mainly malate, are also provided to bacteria by the plant, and are essential for N fixation [1].
During the establishment of the symbiotic relationship, communication signals are exchanged between rhizobia and legumes, involving flavonoids, which are released into the rhizosphere by the plant root [5,6] and trigger the production of lipochitooligosaccharide (LCO) nodulation factors (Nod factors) in compatible rhizobia (reviewed in [7]). Nod factor signaling triggers a response cascade resulting in rhizobial entry into the root epidermis and cortex, paralleled by the formation of a nodule primordium. Nodules are lateral root organs where rhizobia are hosted intracellularly and develop into N-fixing bacteroids surrounded by a plant-derived membrane individually or in small groups, forming organelle-like symbiosomes (reviewed in [8]).
Arbuscular mycorrhizal symbiosis, the association formed between plants and fungi of the phylum Glomeromycota, plays a critical role in nutrient acquisition by providing access predominantly to P, but also to N and other mineral nutrients. AM fungi were found to possess high-affinity transporters of inorganic phosphate (P) [9], which accumulates as polyphosphate within arbuscules and is then rapidly translocated to the host plant [10]. N is also taken up by AM fungi from the substrate, and genes involved in the transfer of NH4+ and amino acids to host plants have been identified [11,12]. AM fungi receive photosynthetic carbon in the form of sugars and lipids (reviewed in [13]) and are obligate biotrophs, strictly relying on host plant resources for growth and reproduction.
Early chemical communication between AM fungi and host plants involves strigolactones released by plant roots [14], and a cocktail of fungal chitooligosaccharides (COs) and lipochitooligosaccharides (LCOs) [15,16]. AM fungal entry into the root is achieved through appressoria that develop on the root epidermal surface [17]. Following hyphal entry, highly branched fungal arbuscules are formed within cells of the inner root cortex. Like symbiosomes in nodules, these are surrounded by a plant plasmalemma-derived membrane and represent the major sites of nutrient exchange between micro- and macrosymbiont [18]. Arbuscules have a limited lifetime, and following their collapse and digestion by the host cell, the latter can be re-colonized by a new arbuscule (reviewed in [19]).

3. Plant Responses to N Availability and Rhizobial Symbiosis Involve CEP and CLE Peptide Regulation

Peptide hormones facilitate both cell-to-cell signaling in plant tissues and systemic communication between organs by long-distance mobility through the vascular system. Plant genomes encode a variety of small signaling peptides (SSPs), which in their mature state are post-translationally modified, small (<20 amino acids) peptides cleaved from a longer precursor protein, and are involved in developmental and physiological processes and mediating plant responses to environmental stimuli. Several SSP gene families show differential abundances in response to changes in plant nutrient status, and have roles in processes controlling root morphogenesis and physiology, as well as macronutrient uptake [20,21]. The CLE (CLAVATA3/EMBRYO SURROUNDING REGION-RELATED) and CEP (C-TERMINALLY ENCODED PEPTIDES) families have been studied extensively in relation to their roles in systemic N signaling. Members of other SSP gene families including CAPE (CAP-DERIVED PEPTIDE), GLV (GOLVEN/ROOT GROWTH FACTOR), IDA (INFLORESCENCE DEFICIENT IN ABCISSION), PIP (PAMP-INDUCED SECRETED PEPTIDE) and TAX (TAXIMIN) encoding genes were similarly suggested to play roles in nutrient-status-related signaling [20]. In the following paragraphs we discuss the roles of CLE and CEP peptides in N deficiency and nodulation symbiosis signaling.

3.1. Roles of CLE Peptides in N Homeostasis and Symbiosis Regulation

CLE peptides are 12 to 13 amino acids long and function as secreted peptide ligands that bind to plasma membrane-localized receptor-like proteins, thereby triggering downstream signaling events. The CLE gene family encodes small proteins with a conserved CLE domain at the C-terminus, generating the mature CLE peptide following proteolytic processing [22]. CLE peptides regulate various physiological and developmental processes, and a number of CLEs were reported to be involved in nutrient homeostasis and to respond to symbiotic interactions with microorganisms [23].
The Arabidopsis thaliana genome harbors 32 CLE genes [22]. Among them, CLE1, -3, -4 and -7 show increased activity in N-deficient compared to sufficient roots and were suggested to regulate lateral root primordia formation through binding to the CLAVATA1 (CLV1) leucine-rich repeat-receptor-like kinase [24]. These CLE genes are expressed in the root pericycle, and the corresponding CLE peptides are hypothesized to be secreted from pericycle cells and transported through the apoplastic continuum within the central cylinder to reach phloem companion cells where CLV1 is localized. The CLE-CLV1 signaling pathway is a key mechanism regulating the outgrowth of lateral roots and the expansion of the root system when A. thaliana plants grow under N-deficient conditions, enhancing the plant survival in N-poor environments [24].
In legume plants, multiple CLE genes have been proposed to be involved in nodulation control. Some legume CLE genes are specifically linked to the rhizobial symbiosis, while others are regulated by both rhizobia and N availability. A number of CLE peptides have been reported to negatively regulate nodulation, acting as essential components of a plant mechanism called autoregulation of nodulation (AON) which balances nodule numbers with plant needs and resource availability (for a recent review see [25]). CLE genes related to rhizobial infection or symbiosis include L. japonicus LjCLE-RS1, -2, -3 and LjCLE40 [26,27], M. truncatula MtCLE12, -13 and -35 [28,29,30], Glycine max GmRIC1 and -2 [31] and Phaseolus vulgaris PvRIC1 and -2 [32] (Figure 1, Table 1). Among them, LjCLE-RS1, MtCLE12, MtCLE13, GmRIC1 and GmRIC2 were reported to specifically show increased expression activity in roots upon rhizobial infection compared to mock treated roots [27,28,31]. Consistent with root–shoot mobility, LjCLE-RS2 derived peptides, though specifically expressed in roots, were found in xylem sap collected from shoot tissue of infected plants [26]. LjCLE-RS2 peptides were further found to directly bind to the shoot-localized CLV1-type leucine-rich repeat receptor-like kinase (LRR-RLK) LjHAR1 (HYPERNODULATION ABERRANT ROOT FORMATION 1) [33], a negative regulator of symbiosis [34,35]. Putative orthologues of LjHAR1 in other legumes, the symbiosis regulators MtSUNN, GmNARK [36] and PvNARK [32] are likely to similarly act as receptors of rhizobia-induced, xylem-mobile CLE peptides.
In a process analogous to AON, root nodulation symbiosis is inhibited by high nitrate concentrations in the environment. LjCLE-RS2 expression is induced by both rhizobial inoculation and nitrate supply, implying a dual role in rhizobia-induced autoregulation and nitrate-mediated inhibition of nodulation [26]. Studies on CLE35 in M. truncatula offer further evidence for an involvement of AON components in nitrate inhibition of nodulation. MtCLE35 is a nitrate-responsive gene, which is also expressed during nodulation [29]. Overexpression of MtCLE35 in transgenic roots of M. truncatula led to reduced root nodule numbers, in a SUNN- dependent manner [30]. Additionally, downregulation of MtCLE35 through RNAi resulted in increased nodule numbers, even under nitrate conditions where nodulation was inhibited in wild-type plants [37]. MtCLE34 was also co-induced by nitrate and rhizobia but turned out to be a pseudogene lacking a functional CLE domain [30]. It was thus proposed that MtCLE34 might have had a role in nodulation, before it was mutated and lost its function [30].
Biochemical studies revealed that CLE peptides are post-translationally modified. In the well-studied CLV3 peptide of A. thaliana, a proline residue at position 7 is hydroxylated and subsequently arabinosylated, a prerequisite for its biological activity and high-affinity binding to its receptor CLV1 [38]. Hydroxyproline O-arabinosylation is widely observed in secreted A. thaliana peptides, and Golgi-localized enzymes encoded by three AtHPAT genes mediate this process [39]. CLE arabinosylation was similarly reported in other plants, such as L. japonicus [33], M. truncatula [40,41] and P. sativum [42], suggesting that this modification may be a requirement for receptor binding and functionality in general. In M. truncatula, the rhizobium-induced MtCLE12 was suggested to be arabinosylated by the Golgi-localized hydroxyproline O-arabinosyltransferase ROOT DETERMINED NODULATION1 (RDN1), as MtCLE12 overexpression did not affect root nodule numbers in rdn1 loss-of-function mutants [40,41]. Interestingly, in contrast to MtCLE12, tri-arabinosylation of MtCLE13 was RDN1-independent, suggesting that other enzymes are also involved in CLE peptide arabinosylation in this species [41]. In L. japonicus, CLE-RS1 and CLE-RS2 tri-arabinosylation was shown to be critical for HAR1 binding and activity in AON [33]. While the enzyme catalyzing glycosylation of these peptides is unclear, a third CLE mediating HAR1-dependent AON in L. japonicus, LjCLE-RS3, was shown to be arabinosylated through LjPLENTY, a putative ortholog of MtRDN1/Pisum sativum NOD3, which are all homologs of AtHPAT genes [43]. Consistently, PLENTY also localizes to the Golgi complex. Overexpression of LjCLE-RS1 and -2 in a plenty mutant background retained AON activity, whereas LjCLE-RS3 mediated repression of nodulation was abolished in plenty mutants [43]. LjCLE-RS1 and -2 are thus likely arabinosylated at least in part by enzymes other than PLENTY [43].
Table
Table 1. List of selected CLE and CEP peptides responding to nitrogen (N), phosphorus (P) and microsymbionts (rhizobium and AM fungi).
Table 1. List of selected CLE and CEP peptides responding to nitrogen (N), phosphorus (P) and microsymbionts (rhizobium and AM fungi).
StimuliOrganismInfluence RangePredominant Expression (Tissue)Refs
AtCLE1
AtCLE3
AtCLE4
AtCLE7		N-deficiency inducedA. thalianasystemicroots[24]
LjCLE-RS1Rhizobium-inducedL. japonicussystemicroots[26]
LjCLE-RS2Rhizobium- and N-inducedL. japonicuslocal and systemicroots[26]
LjCLE-RS3 LjCLE40Rhizobium- and N-inducedL. japonicus roots, nodule primordia[27]
LjCLE19
LjCLE20		P-inducedL. japonicus roots[44]
MtCLE12Rhizobium-inducedM. truncatulalocal and systemicnodules[28]
MtCLE13Rhizobium- and nod factor-induced, cytokinin-inducedM. truncatulalocal and systemicroots (symbiosis susceptible zone), inner cortical cells, nodules[28]
[45]
MtCLE35Rhizobium- and N-inducedM. truncatulasystemicroots, nodules[29]
[30]
MtCLE32Pi-inducedM. truncatula roots[46]
MtCLE33Pi-inducedM. truncatula root vascular tissue[46]
[47]
MtCLE16 MtCLE45AM-inducedM. truncatula roots[46]
[47]
MtCLE53AM-inducedM. truncatula root vascular tissue near colonized regions[46]
[47]
GmRIC1
GmRIC2		Rhizobium-induced G. maxsystemicroots[31]
GmNIC1N-inducedG. maxlocalroots[31]
PvRIC1
PvRIC2		Rhizobium-induced, P-deficiency increasedP. vulgarissystemicroots, pericycle cells of Pi-deficient roots[32]
[48]
AtCEP1
AtCEP3
AtCEP5
AtCEP6
AtCEP7
AtCEP8
AtCEP9		N starvation-inducedA. thalianasystemicmainly roots (but also in aerial tissues)[49]
MtCEP1Rhizobium-induced, N starvation-inducedM. truncatulalocal and systemicroots, shoots[50,51,52]
MtCEP2
MtCEP12		Rhizobium-induced, N starvation-inducedM. truncatula mainly roots, shoots[52]
MtCEP4
MtCEP5
MtCEP6
MtCEP8		N starvation-inducedM. truncatula mainly roots, shoots[52]
MtCEP7Rhizobium- and nod factors-induced, cytokinin-inducedM. truncatulasystemicroots, epidermal cells in colonized roots, nodule primordia, mature nodules[45]
SlCEP2AM-reducedS. lycopersicumlocalroots[53]

3.2. Roles of CEP Peptides in N Homeostasis and Symbiosis Regulation

CEP peptides are a family of SSPs which are 15 amino acids long, secreted peptides released from a C-terminal conserved domain (the CEP domain) of precursor proteins through proteolytic processing. Similarly to CLEs, CEPs are also post-translationally modified by proline hydroxylation and arabinosylation [54]. The accumulation of CEPs was observed to be highly correlated with plant responses to N starvation. The A. thaliana genome includes 11 CEP genes, 7 of which have been shown to be up-regulated specifically in response to N starvation [49]. Moreover, 10 out of the 11 CEP genes led to enhanced expression of the nitrate transporter gene NRT2.1 when overexpressed in A. thaliana seedlings [49].
The well-studied AtCEP1 peptide in A. thaliana was shown to undergo long-distance root-to-shoot translocation and proposed to mediate plant adaptations to low environmental N availability [49]. CEP1 directly binds to the leucine-rich repeat receptor kinases CEPR1 and CEPR2, found to locate in both shoots and roots [49]. The systemic nature of this mechanism was shown via grafting (cepr1-1 cepr2-1 mutant scions were grafted onto wild-type rootstocks by hypocotyl-to-hypocotyl grafting) and split root (the root system of a plant was separated into two parts exposed to different nutrient conditions) studies, and the translocation of CEP1 was verified by its detection in the xylem sap [49]. Exogenous application of CEP1 and CEPR1/2 loss of function studies showed that the CEP1-CEPR1/2 signaling pathway regulates N uptake by affecting the expression of genes encoding for the nitrate transporters NRT1.1, NRT2.1 and NRT3.1 [49].
Similarly to CLE peptides, CEP peptides have been reported to be involved not only in N-deficiency responses but also nodulation control in legumes. In contrast to the repressive role of CLE peptides on symbiotic nodule numbers, CEPs have been attributed a positive regulatory role in nodulation. MtCEP1 in M. truncatula was shown to enhance nodulation when overexpressed or externally applied to Sinorhizobium meliloti-infected roots [50]. Exogenous application of MtCEP1 to M. truncatula roots led to significantly decreased lateral root numbers, while nodule numbers increased [50]. Both effects were mediated by the LRR-RLK CRA2 (COMPACT ROOT ARCHITECTURE 2), the putative orthologue of AtCEPR1 in M. truncatula, as they were abolished in cra2 loss-of-function mutants [51]. In addition to MtCEP1, MtCEP2 and MtCEP12 were N-starvation induced, and co-regulated lateral root and nodule numbers [52] (Table 1). Grafting studies revealed that the CRA2-mediated signaling pathway affecting root architecture is locally active in roots, whereas CRA2-mediated nodulation control is an independent process which is systemically regulated through shoot-localized CRA2 [55]. The systemic MtCEP1-CRA2 node promotes nodulation under low N conditions by regulating the downstream signaling components miR2111 and TML (see below) [56].
MtCEP7, which was reported to be induced by rhizobia, Nod factors and cytokinin [45], seems to function as positive regulators of symbiosis, as exogenous CEP7 application reinforced nodulation, whereas CEP7 downregulation led to reduced nodule numbers [45]. Similarly to MtCEP1, MtCEP7 was also seen to control nodulation through a systemic signaling pathway mediated by the shoot-localized population of the CRA2 receptor [45].
In summary, downstream effects of rhizobium or nitrate-induced CLE and CEP peptides are antagonistic, with CLE peptides mediating restriction, and CEP peptides promoting nodulation. These opposite responses are mediated by partially overlapping signaling pathways sharing common components. Chromatin immunoprecipitation studies revealed that the transcription factor NIN co-regulates the expression of MtCLE13 and MtCEP7, and ectopic expression of MtNIN induced the expression of MtCLE13 and MtCEP7 in the absence of external stimuli [45]. Moreover, both MtCLE13 and MtCEP7 were induced by cytokinin, and the effects of both peptides on nodulation were mediated by the cytokinin receptor gene MtCRE1 [45]. Studies on the crosstalk between peptide and classical hormones provide evidence that peptide signaling is interlinked with signaling through cytokinin, auxin, ethylene and strigolactones (for a recent review see [57]). The concurrent induction of the antagonistic CLE and CEP pathways may be part of a mechanism that enables the plant to flexibly adjust rhizobial infection events and the nodule numbers to its needs based on the endogenous supply status of various nutrients, photosynthetic capacity and environmental conditions.

4. CLEs and CEPs Respond to Both P and AM Fungal Infection

In contrast to root nodulation symbiosis, where host plants are supplied with bacterially fixed aerial N, AM fungi predominantly deliver phosphate extracted from the surrounding substrate to the host. It was shown that high exogenous phosphate supply restricts the initiation and development of AM symbiosis. P acts systemically to repress symbiotic gene expression and AM fungal root colonization [58].
Analogous to CLE-mediated regulation of nodulation symbiosis, this regulation of AM involves CLE peptides (Table 1, Figure 1). In M. truncatula, expression of MtCLE32 and MtCLE33 was significantly induced in roots grown under high (2 mM) P conditions compared to P-starved roots [46]. Further, ectopic overexpression of the MtCLE33 in M. truncatula transgenic roots resulted in reduced AM root colonization [46]. Apart from peptides, phytohormones and miRNAs have been reported to have key roles in P starvation and AM symbiosis signaling, regulating the initiation, maintenance, and extent of AM root colonization (reviewed in [59]).
The development of AM fungi within the root is regulated by the host plant through a genetic mechanism termed autoregulation of mycorrhizal symbiosis (AOM) [60], a systemic signaling cascade sharing common elements with AON [61]. Along this line, it was shown that root-derived CLE peptides and a CLV1-type shoot-localized receptor regulate the colonization of roots by AM fungi [46,47]. Transcript abundance of specific CLE genes was found to increase upon AM fungal root colonization [46,47,62]. Certain CLE genes responding to AM symbiosis were also shown to respond to phosphate availability [47] (Table 1, Figure 1), reminiscent of the dual regulation of CLE genes by rhizobial infection and nitrate [26,27]. Ectopic overexpression of the AM-induced MtCLE53 in the roots of M. truncatula resulted in reduced fungal colonization compared to control roots [46,47], whereas cle53 mutants showed higher colonization levels than wild-type plants [47]. Interestingly, the nodulation-induced MtCLE13 [28] was not induced by AM symbiosis, and ectopic overexpression of MtCLE13 seems not to have an effect on fungal colonization levels, implying specificity of the respective CLEs [46].
Similarly to AON, arabinosylation of CLE peptides may also be a requirement for receptor binding and functionality in AOM. Karlo et al. [47] showed that the hydroxyproline O-arabinosyltransferase RDN1 has a role in the control of fungal colonization in M. truncatula. Mycorrhized roots of rdn1 mutants contained more vesicles and arbuscules than wild-type roots. In line with a requirement for RDN1-mediated arabinosylation of MtCLE53, overexpression of the latter in an rdn1 genetic background did not reduce AM fungal colonization as in wild-type plants [47].
Although CLE peptides may respond to diverse stimuli, the shoot-localized receptor LjHAR1/MtSUNN/GmNARK/PsSYM29, may be a common component of the respective signaling mechanisms (discussed in [57]). In M. truncatula, downstream signaling of the AM-induced MtCLE53, the rhizobium-induced MtCLE13 or the P-responsive MtCLE33 was dependent on SUNN in overexpression assays, implying SUNN as a common receptor for all three CLE peptides [45,46]. Components acting downstream of the shoot receptor in AOM are still unknown, except that it was shown that the control of fungal root colonization in M. truncatula seems mediated by regulation of strigolactone biosynthesis via M. truncatula DWARF27 (MtD27) expression [63]. This regulation was shown to be dependent on P levels and AM signaling, and was mediated by SUNN and CLEs [46].
In addition to CLE peptides, a genome-wide investigation of SSPs in M. truncatula found CEPs to be responsive to P deficiency [21]. Further, recent findings showed CEP2 to be downregulated in AM-inoculated S. lycopersicum roots. SlCEP2 was proposed to promote lateral root formation in tomato plants through an auxin-related pathway, which might be CEPR1-mediated [53]. However, so far, no direct evidence of a functional involvement of CEPs in AOM has been reported, and a putative function in AM control will be an interesting subject of future studies.

5. miRNAs Respond to N and P Availability and Symbiosis-Mediated Nutrient Acquisition

MicroRNAs are small, non-coding RNA molecules, typically 21–24 nucleotides in length, that exert post-transcriptional gene regulation by homology-based pairing to target mRNAs, inducing their degradation or translational inhibition.
Several miRNAs have been associated with responses to N availability in different plant species (Table 2, Figure 1). In A. thaliana, upon N starvation, the expression of one or more miRNAs of the miR169, miR171 and miR395 families was repressed, while miR160 and miR780 expression was induced [64]. In addition, an A. thaliana miR167 isoform was the first miRNA to be linked to plant N-responses, and was shown to mediate N dependent lateral root outgrowth [65]. More studies in A. thaliana, but also other plants, have shown that the regulation of the plant root architecture is a major function of N-responsive miRNAs. Interestingly, both miR167 and miR393 influence root architecture by interfering with auxin signaling through targeting the AUXIN RESPONSE FACTOR 8 (ARF8) [65] and the AUXIN-SIGNALING F-BOX PROTEIN 3 (AFB3) [66], respectively. Further, miR169 targets the transcript of NFYA5, which encodes a transcription factor suggested to regulate N-starvation responses in plants by affecting the expression of the nitrate transporters AtNRT1.1 and AtNRT2.1 [67]. Interestingly, apart from miRNAs, also long non-coding RNAs (lncRNAs) have been found to respond to the N status in different plants (for a recent review see [68]).
Consistent with a general role of miRNAs in maintaining plant nutrient homeostasis, several miRNAs have further been reported to respond to P availability (Table 2, Figure 1). Among them, miR399, miR827 and miR2111 isoforms were found to accumulate under P-starvation conditions in different plant species including A. thaliana and N. benthamiana. These miRNAs were present in the phloem sap of P-starved B. napus plants, suggesting organ-to-organ mobility along with long-distance regulation of gene expression [69,70,71]. A well-studied P-responsive miRNA is miR399, which undergoes long-distance shoot-to-root allocation during the onset of P deficiency [69] and is suggested to mediate enhanced P uptake and translocation [72]. miR399 post-transcriptionally regulates PHO2 (PHOSPHATE 2), a ubiquitin-conjugating E2 enzyme that targets members of the PHT1 (PHOSPHATE TRANSPORTER 1) family for ubiquitin-mediated degradation [69,72,73,74].
Phosphate starvation and AM-symbiosis-related signaling networks interlink, and miRNAs are among the shared components. For example, the miR399-PHO2 node-regulating P-homeostasis in non-mycorrhizal plants was shown to be acting in AM-colonized roots of M. truncatula [75]. Studies in different symbiotic plants have identified miRNAs that dually respond to P availability and AM fungal infection. For example, miR393, shown to restrict arbuscule development by targeting auxin receptors involved in arbuscule formation, is induced by low P-concentrations and repressed by AM [76]. The responsiveness of different miRNAs in the environmental P conditions and their roles in AM symbiosis are reviewed in [59]. A particularly interesting antagonistic role is reported for miR171 isoforms in M. truncatula AM symbiosis control. Several miR171 family members negatively regulate root invasion by AM fungi via post-transcriptional control of the GRAS-type transcription factor LOM (LOST MERISTEMS 1), a positive regulator of AM [77]. In contrast, miR171b, which specifically accumulates in arbuscule-containing plant cells, displays a mismatched cleavage site and prevents cleavage of LOM1 transcripts by other members of the miR171 family [77].
M. truncatula miR171h (L. japonicus miR171c), which targets the GRAS-type transcription factor NODULATION SIGNALLING PATHWAY2 (NSP2) transcripts [78,79], accumulates under both N and P sufficiency and has been reported to be involved in both rhizobial nodulation and AM symbioses. NSP2 is essential for nodulation in legumes [80,81], and positively regulates AM fungal colonization [15]. It is further involved in strigolactone biosynthesis [82]. In line with its roles in symbiosis development, M. truncatula miR171h accumulation is not only nutrient-status-dependent, but also induced by myc-LCO and nod factor signaling during AM and nodulation symbioses [78,79,83]. Ectopic overexpression of pri-miR171h in M. truncatula roots resulted in reduced mycorrhizal root colonization and nodule numbers compared to controls, when plants were inoculated with AM fungi and rhizobia, respectively [83]. Thus miR171h seems to have a central role in integrating plant responses to the essential nutrients N and P, and the acquisition of these nutrients through symbiotic associations.
Several miRNAs have been reported to respond to rhizobial inoculation (Table 2, Figure 1) and are presumed to play roles during early stages of the symbiotic interaction, mostly by targeting transcripts of genes encoding transcription factors. Apart from miR171 family members, these include miR319d in common beans and miR172 in many plant species (reviewed in [84]). The sequencing of sRNA libraries from nodules alongside a degradome analysis identified several miRNA-target pairs that show activity in nodules. In soybeans, combined sRNA and degradome sequencing revealed miR167 targeting the 5’UTR of the nuclear cation channel CYCLOPS as well as miR393j-3p targeting of ENOD93 (EARLY NODULIN 93) [85]. The overexpression of miR393 in soybean roots significantly reduced nodulation [85]. M. truncatula miR167 family members further target auxin response factors [86], and L. japonicus miR397 targets a Cu2+-containing LACCASE [79]. The regulation of some miRNAs has been linked to auxin and cytokinin action in the legume–rhizobium symbiosis, however there are only a few studies on this topic (reviewed in [84]). Interestingly, in line with an adaptation of conserved developmental mechanisms in the genetic regulation of symbiosis, M. truncatula miR166 has a dual role regulating root and nodule development. miR166 isoforms target HD-ZIPIII (CLASS-III HOMEODOMAIN-LEUCINE ZIPPER) genes, a family of transcription factors associated with nodule development, and overexpression of MtMIR166 affected both nodule and lateral root numbers as well as vascular bundle development [87].
Over the last years, miR2111 has emerged as a key component of root nodulation control via the AON mechanism (discussed in Section 6 of the current article). miR2111 is a mobile signal undergoing shoot-to-root translocation. It accumulates in shoots under low N conditions and acts as a positive regulator of nodulation by targeting root-localized transcripts encoding the F-Box Kelch-repeat protein TML (TOO MUCH LOVE) [88], an inhibitor of rhizobial infection and nodulation [89,90].
A second miRNA implemented in AON is soybean miR172c [91,92]. miR172c strongly accumulates in the vicinity of rhizobial invasion and in nodules [91,93] and acts as a positive regulator of rhizobial infection and nodule formation through regulation of AP2/ERF transcription factor mRNAs [91,93]. In soybeans, the transcriptional repressor NNC1 (NODULE NUMBER CONTROL 1) is assumed to be the primary miR172 target [91,92]. NNC1 is a negative regulator of nodulation and was shown to bind to the promoters of the early nodulin genes ENOD40-1 and -2, inhibiting their expression. NNC1 further interacts with NIN (NODULE INCEPTION), inhibiting the transcription of downstream genes encoding GmRIC1 and GmRIC2 peptides, linking it to AON. Using a nark loss-of-function mutant, it was shown that miR172c is negatively regulated by NARK, an observation providing additional evidence for the involvement of the miR172c-NNC1 node in AON in soybeans [91,92].
Table
Table 2. List of selected miRNAs responding to nitrogen (N), phosphorus (P) and microsymbionts (rhizobium and AM fungi).
Table 2. List of selected miRNAs responding to nitrogen (N), phosphorus (P) and microsymbionts (rhizobium and AM fungi).
StimuliOrganismInfluenceTissueTargetRefs
miR167N-repressedA. thalianalocalroot pericycle cellsARF8[65]
miR169 N-limitation repressed A. thaliana and B. napussystemicshoots, roots, phloem sapNFYA5[67]
[70]
miR398aN-limitation and
P-limitation repressed		A. thaliana [70]
miR399P-limitation inducedA. thaliana
and B. napus		systemicvascular tissues, phloem sapPHO2[70]
[72]
miR2111P-limitation induced
N-repressed, rhizobium-repressed		A. thaliana and B. napus
L. japonicus		systemicphloem sap
leaves phloem, phloem sap		E3 ligase
TML		[76]
[88]
miR397nodulation-inducedL. japonicuslocal and systemicnodules, leavesLACCASE10[79]
miR171cnodulation-inducedL. japonicus nodulesNSP2[79]
miR171hexpressed in high P and N, AM-repressed, nodulation-inducedM. truncatula roots, arbuscule-containing cells, nodulesNSP2[83]
miR171bAM-specificM. truncatulalocalcolonized root cellsLOM1[77]
miR393low-P expressed,
AM-repressed		M. truncatulalocalrootsauxin receptors[76]
miR399low P-induced, AM-induced M. truncatulasystemicleaves and rootsPHO2[75]
miR166nodulation inducedM. truncatulalocalvascular bundles, roots, nodulesHD-ZIP III[87]
miR172crhizobium-induced, nod factors-induced G. maxlocalrhizobium-inoculated roots and nodules NNC1[91]
miR156b rhizobium-repressedG. maxlocalrootsGmSPL9d[94]
In a recent report, Yun et al. [94] showed that overexpression of miR156b in soybean roots resulted in reduced expression of NINa, ENOD40-1 and MIR172c. The main target of miR156b is the GmSPL9d (SQUAMOSA PROMOTER-BINDING LIKE 9d) gene, a positive regulator of symbiosis that accumulates upon infection. GmSPL9d affects the expression of NINa, ENOD40-1 and MIR172c by direct promoter binding [94]. Similarly, in L. japonicus, ectopic overexpression of miR156a reduced nodulation and affected the expression of early nodulation genes such as ENOD genes, NFR1, CYCLOPS and NSP1 [95]. These data suggest that the miR156-SPL node has a key regulatory role in nodulation by directly activating the expression of core genes in the early stages of nodulation signaling.

6. CEPs and CLEs and miR2111 Jointly Orchestrate Plant Responses to N and Rhizobia

AON controls rhizobial infection and nodule numbers to ensure a viable balance between ammonia uptake and carbohydrate as well as nutrient costs. This feedback loop has been well-described in different plant species and was shown to be systemic, involving CLE and CEP peptides as root-derived signals moving to the shoot through the xylem, and micro RNA miR2111 as well as CEPD peptides as shoot-derived, root-active signals navigating through the phloem [56,88]. miR2111 is mainly expressed in shoot tissues, more precisely in leaf vein phloem [88,96]. Leaf phloem expression was postulated as prerequisite for systemic mobility of small RNAs [97], and indeed, miR2111 was shown to translocate from shoot to root [88,96]. Shoot-derived miR2111 effectively reduces root transcript levels of TML via endonucleolytic cleavage [88].
The miR2111-TML node is responsive to both soil nitrate levels and rhizobial signaling, suggesting a role in balancing nodulation symbiosis with N availability. Nitrate fertilization or rhizobial inoculation led to decreased miR2111 levels, and accordingly, TML transcript abundance increased [56,88].
miR2111 expression depends on two peptide receptors, the LRR-RLKs LjHAR1/MtSUNN/GmNARK and MtCRA2 [37,56,88,96]. Both factors are expressed in the whole plant, however the regulation of symbiosis is mainly achieved by the shoot fraction. HAR1, a negative regulator of symbiosis, represses miR2111 levels in rhizobially infected plants, resulting in TML transcript accumulation and restriction of further infections [88,96]. The second regulator of miR2111, CRA2, is a positive regulator of symbiosis and promotes miR2111 accumulation under low N conditions [56]. The antagonistic regulation of infection through miR2111 underlines the biological relevance of this node. For the plant, both miR2111 promotion and repression, and a fast switch of these states, seem equally important, allowing the plant to quickly change from a susceptible status welcoming infection to restriction of the latter.
Consistent with the divergent effects of activated HAR1/SUNN/NARK and CRA2 on miR2111 regulation, these two shoot receptors differ in the groups of peptide ligands they perceive. HAR1/SUNN/NARK interacts with CLE peptides [29,33], and several studies suggest that the receptor regulates miR2111 depending on root-derived CLE peptide perception [37,88,96]. For example, nitrate induction of MtCLE35 coincided with reduced miR2111 levels and, consistently, an accumulation of MtTML2 transcripts downstream of the SUNN receptor [37]. CRA2, in contrast, perceives CEP peptide ligands, positively regulating miR2111 depending on the presence of CEPs [56]. Overexpression of MtCEP1, for example, resulted in increased miR2111 abundance and reduced transcript levels of both M. truncatula TML1 and TML2 in roots. This was dependent on CRA2, as those effects were not apparent in cra2 mutants [56]. Both classes of peptides possess several members regulated by N and/or symbiosis signaling (see Section 3 of the current article) (Table 1, Figure 1). The combined results indicate that a multitude of CEP and CLE peptide signals triggering divergent responses converge in the miR2111-TML regulon, shaping a model of AON as a complex, multilayered network that dynamically integrates infection and symbiosis development with plant nutritional status and needs.

7. CLE Peptide Involvement in P-Dependent Control of Nodulation

P supply is well known to positively correlate with nodulation and symbiotic N fixation in legumes [98,99], and consistently, nodule fresh weight and activity are sensitive to P deficiency [100]. A study in the actinorhizal plant Alnus incana showed that a high phosphate concentration can reverse the nitrate-induced inhibition of nodulation, leading to an increase of nodules. The positive effect of P on nodule numbers was found to be systemically regulated and independent of overall plant growth and development [101]. In common beans, P deficiency reduced the numbers of the bacterially induced root hair deformations during the initial steps of rhizobial infection [102]. Although a negative effect of P deficiency on nodulation has been clearly documented, the underlying molecular mechanisms were unknown until recently.
In the roots of common beans, P deficiency induced the expression of genes encoding the AON-related root-to-shoot signals RIC1 and RIC2 in the absence of symbiosis [48] (Table 1). Moreover, it was shown that, under P deficiency, RIC1 and RIC2 led to a systemic restriction of nodulation, through the HAR1/SUNN/NARK receptor in both common beans and soybeans. This effect seems to be mediated by TML, as TML transcripts accumulated in the roots of both plants [48]. These data suggest that CLE peptides negatively regulate nodule formation under P deficiency conditions via the AON genetic network.

8. Conclusions

Plants have adopted different strategies to control nutrient homeostasis and overcome nutrient limitation in their environment, such as the adaptation of root system architecture and the establishment of root symbiotic relationships.
The molecular basis of these response systems has been the subject of intense interest by the scientific community in the light of reducing dependence on inorganic fertilizers while securing global food supplies. Studies in model plants revealed conserved processes that ensure survival and productivity under nutrient deprivation, and there is an increasing host of knowledge on how plants cope with fluctuations in the availability of important nutrients such as N and P in the soil. However, more research to this field is not only important for transferring the knowledge acquired in model systems to a wider range of species including crop plants, but also to grasp the relevance of these processes in natural communities, and in adapting plant populations to increasingly challenging environmental conditions in the face of climate change.

Author Contributions

Conceptualization, D.T.; writing—original draft preparation, M.I.V. and M.S.; writing—review and editing, D.T. and K.M.; supervision, D.T. and K.M. All authors have read and agreed to the published version of the manuscript.

Funding

This work received no external funding.

Data Availability Statement

Not applicable.

Conflicts of Interest

The authors declare no conflict of interest.

References

  1. Udvardi, M.; Poole, P.S. Transport and Metabolism in Legume-Rhizobia Symbioses. Annu. Rev. Plant Biol. 2013, 64, 781–805. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  2. Patriarca, E.J.; Tatè, R.; Iaccarino, M. Key Role of Bacterial NH4+ Metabolism in Rhizobium-Plant Symbiosis. Microbiol. Mol. Biol. Rev. 2002, 66, 203–222. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  3. Kaiser, B.N.; Finnegan, P.M.; Tyerman, S.D.; Whitehead, L.F.; Bergersen, F.J.; Day, D.A.; Udvardi, M.K. Characterization of an Ammonium Transport Protein from the Peribacteroid Membrane of Soybean Nodules. Science 1998, 281, 1202–1206. [Google Scholar] [CrossRef] [PubMed]
  4. Salvemini, F.; Marini, A.; Riccio, A.; Patriarca, E.J.; Chiurazzi, M. Functional Characterization of an Ammonium Transporter Gene from Lotus japonicus. Gene 2001, 270, 237–243. [Google Scholar] [CrossRef]
  5. Maxwell, C.A.; Hartwig, U.A.; Joseph, C.M.; Phillips, D.A. A Chalcone and Two Related Flavonoids Released from Alfalfa Roots Induce Nod Genes of Rhizobium Meliloti. Plant Physiol. 1989, 91, 842–847. [Google Scholar] [CrossRef] [Green Version]
  6. Long, S.R.; Staskawicz, B.J. Prokaryotic Plant Parasites. Cell 1993, 73, 921–935. [Google Scholar] [CrossRef]
  7. Dénarié, J.; Debellé, F.; Promé, J.C. Rhizobium Lipo-Chitooligosaccharide Nodulation Factors: Signaling Molecules Mediating Recognition and Morphogenesis. Annu. Rev. Biochem. 1996, 65, 503–535. [Google Scholar] [CrossRef]
  8. Oldroyd, G.E.D.; Murray, J.D.; Poole, P.S.; Downie, J.A. The Rules of Engagement in the Legume-Rhizobial Symbiosis. Annu. Rev. Genet. 2011, 45, 119–144. [Google Scholar] [CrossRef]
  9. Harrison, M.J.; van Buuren, M.L. A Phosphate Transporter from the Mycorrhizal Fungus Glomus Versiforme. Nature 1995, 378, 626–629. [Google Scholar] [CrossRef]
  10. Hijikata, N.; Murase, M.; Tani, C.; Ohtomo, R.; Osaki, M.; Ezawa, T. Polyphosphate Has a Central Role in the Rapid and Massive Accumulation of Phosphorus in Extraradical Mycelium of an Arbuscular Mycorrhizal Fungus. New Phytol. 2010, 186, 285–289. [Google Scholar] [CrossRef]
  11. López-Pedrosa, A.; González-Guerrero, M.; Valderas, A.; Azcón-Aguilar, C.; Ferrol, N. GintAMT1 Encodes a Functional High-Affinity Ammonium Transporter That Is Expressed in the Extraradical Mycelium of Glomus Intraradices. Fungal Genet. Biol. 2006, 43, 102–110. [Google Scholar] [CrossRef] [PubMed]
  12. Cappellazzo, G.; Lanfranco, L.; Fitz, M.; Wipf, D.; Bonfante, P. Characterization of an Amino Acid Permease from the Endomycorrhizal Fungus Glomus Mosseae. Plant Physiol. 2008, 147, 429–437. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  13. MacLean, A.M.; Bravo, A.; Harrison, M.J. Plant Signaling and Metabolic Pathways Enabling Arbuscular Mycorrhizal Symbiosis. Plant Cell 2017, 29, 2319–2335. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  14. Akiyama, K.; Matsuzaki, K.; Hayashi, H. Plant Sesquiterpenes Induce Hyphal Branching in Arbuscular Mycorrhizal Fungi. Nature 2005, 435, 824–827. [Google Scholar] [CrossRef]
  15. Maillet, F.; Poinsot, V.; André, O.; Puech-Pagès, V.; Haouy, A.; Gueunier, M.; Cromer, L.; Giraudet, D.; Formey, D.; Niebel, A.; et al. Fungal Lipochitooligosaccharide Symbiotic Signals in Arbuscular Mycorrhiza. Nature 2011, 469, 58–63. [Google Scholar] [CrossRef]
  16. Genre, A.; Chabaud, M.; Balzergue, C.; Puech-Pagès, V.; Novero, M.; Rey, T.; Fournier, J.; Rochange, S.; Bécard, G.; Bonfante, P.; et al. Short-Chain Chitin Oligomers from Arbuscular Mycorrhizal Fungi Trigger Nuclear Ca2+ Spiking in Medicago truncatula Roots and Their Production Is Enhanced by Strigolactone. New Phytol. 2013, 198, 190–202. [Google Scholar] [CrossRef]
  17. Nagahashi, G.; Douds, D.D., Jr. Appressorium Formation by AM Fungi on Isolated Cell Walls of Carrot Roots. New Phytol. 1997, 136, 299–304. [Google Scholar] [CrossRef]
  18. Bonfante, P.; Genre, A. Mechanisms Underlying Beneficial Plant–Fungus Interactions in Mycorrhizal Symbiosis. Nat. Commun. 2010, 1, 48. [Google Scholar] [CrossRef] [Green Version]
  19. Gutjahr, C.; Parniske, M. Cell Biology: Control of Partner Lifetime in a Plant–Fungus Relationship. Curr. Biol. 2017, 27, R420–R423. [Google Scholar] [CrossRef] [Green Version]
  20. de Bang, T.C.; Lay, K.S.; Scheible, W.-R.; Takahashi, H. Small Peptide Signaling Pathways Modulating Macronutrient Utilization in Plants. Curr. Opin. Plant Biol. 2017, 39, 31–39. [Google Scholar] [CrossRef]
  21. de Bang, T.C.; Lundquist, P.K.; Dai, X.; Boschiero, C.; Zhuang, Z.; Pant, P.; Torres-Jerez, I.; Roy, S.; Nogales, J.; Veerappan, V.; et al. Genome-Wide Identification of Medicago Peptides Involved in Macronutrient Responses and Nodulation. Plant Physiol. 2017, 175, 1669–1689. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  22. Betsuyaku, S.; Sawa, S.; Yamada, M. The Function of the CLE Peptides in Plant Development and Plant-Microbe Interactions. Arab. Book 2011, 9, e0149. [Google Scholar] [CrossRef] [Green Version]
  23. Yamaguchi, Y.L.; Ishida, T.; Sawa, S. CLE Peptides and Their Signaling Pathways in Plant Development. J. Exp. Bot. 2016, 67, 4813–4826. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  24. Araya, T.; Miyamoto, M.; Wibowo, J.; Suzuki, A.; Kojima, S.; Tsuchiya, Y.N.; Sawa, S.; Fukuda, H.; von Wirén, N.; Takahashi, H. CLE-CLAVATA1 Peptide-Receptor Signaling Module Regulates the Expansion of Plant Root Systems in a Nitrogen-Dependent Manner. Proc. Natl. Acad. Sci. USA 2014, 111, 2029–2034. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  25. Chaulagain, D.; Frugoli, J. The Regulation of Nodule Number in Legumes Is a Balance of Three Signal Transduction Pathways. Int. J. Mol. Sci. 2021, 22, 1117. [Google Scholar] [CrossRef]
  26. Okamoto, S.; Ohnishi, E.; Sato, S.; Takahashi, H.; Nakazono, M.; Tabata, S.; Kawaguchi, M. Nod Factor/Nitrate-Induced CLE Genes That Drive HAR1-Mediated Systemic Regulation of Nodulation. Plant Cell Physiol. 2009, 50, 67–77. [Google Scholar] [CrossRef] [Green Version]
  27. Nishida, H.; Handa, Y.; Tanaka, S.; Suzaki, T.; Kawaguchi, M. Expression of the CLE-RS3 Gene Suppresses Root Nodulation in Lotus japonicus. J. Plant Res. 2016, 129, 909–919. [Google Scholar] [CrossRef] [Green Version]
  28. Mortier, V.; Den Herder, G.; Whitford, R.; Van de Velde, W.; Rombauts, S.; D’Haeseleer, K.; Holsters, M.; Goormachtig, S. CLE Peptides Control Medicago truncatula Nodulation Locally and Systemically. Plant Physiol. 2010, 153, 222–237. [Google Scholar] [CrossRef] [Green Version]
  29. Lebedeva, M.; Azarakhsh, M.; Yashenkova, Y.; Lutova, L. Nitrate-Induced CLE Peptide Systemically Inhibits Nodulation in Medicago truncatula. Plants 2020, 9, 1456. [Google Scholar] [CrossRef]
  30. Mens, C.; Hastwell, A.H.; Su, H.; Gresshoff, P.M.; Mathesius, U.; Ferguson, B.J. Characterisation of Medicago truncatula CLE34 and CLE35 in Nitrate and Rhizobia Regulation of Nodulation. New Phytol. 2021, 229, 2525–2534. [Google Scholar] [CrossRef]
  31. Reid, D.E.; Ferguson, B.J.; Gresshoff, P.M. Inoculation- and Nitrate-Induced CLE Peptides of Soybean Control NARK-Dependent Nodule Formation. Mol. Plant-Microbe Interact. 2011, 24, 606–618. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  32. Ferguson, B.J.; Li, D.; Hastwell, A.H.; Reid, D.E.; Li, Y.; Jackson, S.A.; Gresshoff, P.M. The Soybean (Glycine max) Nodulation-Suppressive CLE Peptide, GmRIC1, Functions Interspecifically in Common White Bean (Phaseolus vulgaris), but Not in a Supernodulating Line Mutated in the Receptor PvNARK. Plant Biotechnol. J. 2014, 12, 1085–1097. [Google Scholar] [CrossRef] [PubMed]
  33. Okamoto, S.; Shinohara, H.; Mori, T.; Matsubayashi, Y.; Kawaguchi, M. Root-Derived CLE Glycopeptides Control Nodulation by Direct Binding to HAR1 Receptor Kinase. Nat. Commun. 2013, 4, 2191. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  34. Krusell, L.; Madsen, L.H.; Sato, S.; Aubert, G.; Genua, A.; Szczyglowski, K.; Duc, G.; Kaneko, T.; Tabata, S.; de Bruijn, F.; et al. Shoot Control of Root Development and Nodulation Is Mediated by a Receptor-like Kinase. Nature 2002, 420, 422–426. [Google Scholar] [CrossRef]
  35. Nishimura, R.; Hayashi, M.; Wu, G.-J.; Kouchi, H.; Imaizumi-Anraku, H.; Murakami, Y.; Kawasaki, S.; Akao, S.; Ohmori, M.; Nagasawa, M.; et al. HAR1 Mediates Systemic Regulation of Symbiotic Organ Development. Nature 2002, 420, 426–429. [Google Scholar] [CrossRef]
  36. Searle, I.R.; Men, A.E.; Laniya, T.S.; Buzas, D.M.; Iturbe-Ormaetxe, I.; Carroll, B.J.; Gresshoff, P.M. Long-Distance Signaling in Nodulation Directed by a CLAVATA1-like Receptor Kinase. Science 2003, 299, 109–112. [Google Scholar] [CrossRef] [Green Version]
  37. Moreau, C.; Gautrat, P.; Frugier, F. Nitrate-Induced CLE35 Signaling Peptides Inhibit Nodulation through the SUNN Receptor and MiR2111 Repression. Plant Physiol. 2021, 185, 1216–1228. [Google Scholar] [CrossRef]
  38. Ohyama, K.; Shinohara, H.; Ogawa-Ohnishi, M.; Matsubayashi, Y. A Glycopeptide Regulating Stem Cell Fate in Arabidopsis Thaliana. Nat. Chem. Biol. 2009, 5, 578–580. [Google Scholar] [CrossRef]
  39. Ogawa-Ohnishi, M.; Matsushita, W.; Matsubayashi, Y. Identification of Three Hydroxyproline O-Arabinosyltransferases in Arabidopsis Thaliana. Nat. Chem. Biol. 2013, 9, 726–730. [Google Scholar] [CrossRef]
  40. Kassaw, T.; Nowak, S.; Schnabel, E.; Frugoli, J. ROOT DETERMINED NODULATION1 Is Required for M. Truncatula CLE12, But Not CLE13, Peptide Signaling through the SUNN Receptor Kinase. Plant Physiol. 2017, 174, 2445–2456. [Google Scholar] [CrossRef]
  41. Imin, N.; Patel, N.; Corcilius, L.; Payne, R.J.; Djordjevic, M.A. CLE Peptide Tri-Arabinosylation and Peptide Domain Sequence Composition Are Essential for SUNN-Dependent Autoregulation of Nodulation in Medicago truncatula. New Phytol. 2018, 218, 73–80. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  42. Hastwell, A.H.; Corcilius, L.; Williams, J.T.; Gresshoff, P.M.; Payne, R.J.; Ferguson, B.J. Triarabinosylation Is Required for Nodulation-Suppressive CLE Peptides to Systemically Inhibit Nodulation in Pisum Sativum. Plant Cell Environ. 2019, 42, 188–197. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  43. Yoro, E.; Nishida, H.; Ogawa-Ohnishi, M.; Yoshida, C.; Suzaki, T.; Matsubayashi, Y.; Kawaguchi, M. PLENTY, a Hydroxyproline O-Arabinosyltransferase, Negatively Regulates Root Nodule Symbiosis in Lotus japonicus. J. Exp. Bot. 2019, 70, 507–517. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  44. Funayama-Noguchi, S.; Noguchi, K.; Yoshida, C.; Kawaguchi, M. Two CLE Genes Are Induced by Phosphate in Roots of Lotus japonicus. J. Plant Res. 2011, 124, 155–163. [Google Scholar] [CrossRef] [PubMed]
  45. Laffont, C.; Ivanovici, A.; Gautrat, P.; Brault, M.; Djordjevic, M.A.; Frugier, F. The NIN Transcription Factor Coordinates CEP and CLE Signaling Peptides That Regulate Nodulation Antagonistically. Nat. Commun. 2020, 11, 3167. [Google Scholar] [CrossRef] [PubMed]
  46. Müller, L.M.; Flokova, K.; Schnabel, E.; Sun, X.; Fei, Z.; Frugoli, J.; Bouwmeester, H.J.; Harrison, M.J. A CLE-SUNN Module Regulates Strigolactone Content and Fungal Colonization in Arbuscular Mycorrhiza. Nat. Plants 2019, 5, 933–939. [Google Scholar] [CrossRef] [PubMed]
  47. Karlo, M.; Boschiero, C.; Landerslev, K.G.; Blanco, G.S.; Wen, J.; Mysore, K.S.; Dai, X.; Zhao, P.X.; de Bang, T.C. The CLE53-SUNN Genetic Pathway Negatively Regulates Arbuscular Mycorrhiza Root Colonization in Medicago truncatula. J. Exp. Bot. 2020, 71, 4972–4984. [Google Scholar] [CrossRef] [PubMed]
  48. Isidra-Arellano, M.C.; Pozas-Rodríguez, E.A.; Del Rocío Reyero-Saavedra, M.; Arroyo-Canales, J.; Ferrer-Orgaz, S.; Del Socorro Sánchez-Correa, M.; Cardenas, L.; Covarrubias, A.A.; Valdés-López, O. Inhibition of Legume Nodulation by Pi Deficiency Is Dependent on the Autoregulation of Nodulation (AON) Pathway. Plant J. 2020, 103, 1125–1139. [Google Scholar] [CrossRef] [PubMed]
  49. Tabata, R.; Sumida, K.; Yoshii, T.; Ohyama, K.; Shinohara, H.; Matsubayashi, Y. Perception of Root-Derived Peptides by Shoot LRR-RKs Mediates Systemic N-Demand Signaling. Science 2014, 346, 343–346. [Google Scholar] [CrossRef]
  50. Imin, N.; Mohd-Radzman, N.A.; Ogilvie, H.A.; Djordjevic, M.A. The Peptide-Encoding CEP1 Gene Modulates Lateral Root and Nodule Numbers in Medicago truncatula. J. Exp. Bot. 2013, 64, 5395–5409. [Google Scholar] [CrossRef]
  51. Laffont, C.; Huault, E.; Gautrat, P.; Endre, G.; Kalo, P.; Bourion, V.; Duc, G.; Frugier, F. Independent Regulation of Symbiotic Nodulation by the SUNN Negative and CRA2 Positive Systemic Pathways. Plant Physiol. 2019, 180, 559–570. [Google Scholar] [CrossRef] [PubMed]
  52. Zhu, F.; Ye, Q.; Chen, H.; Dong, J.; Wang, T. Multigene Editing Reveals That MtCEP1/2/12 Redundantly Control Lateral Root and Nodule Number in Medicago truncatula. J. Exp. Bot. 2021, 72, 3661–3676. [Google Scholar] [CrossRef] [PubMed]
  53. Hsieh, Y.-H.; Wei, Y.-H.; Lo, J.-C.; Pan, H.-Y.; Yang, S.-Y. Arbuscular Mycorrhizal Symbiosis Enhances Tomato Lateral Root Formation by Modulating CEP2 Peptide Expression. New Phytol. 2022, 235, 292–305. [Google Scholar] [CrossRef] [PubMed]
  54. Ohyama, K.; Ogawa, M.; Matsubayashi, Y. Identification of a Biologically Active, Small, Secreted Peptide in Arabidopsis by in Silico Gene Screening, Followed by LC-MS-Based Structure Analysis. Plant J. 2008, 55, 152–160. [Google Scholar] [CrossRef]
  55. Huault, E.; Laffont, C.; Wen, J.; Mysore, K.S.; Ratet, P.; Duc, G.; Frugier, F. Local and Systemic Regulation of Plant Root System Architecture and Symbiotic Nodulation by a Receptor-like Kinase. PLoS Genet. 2014, 10, e1004891. [Google Scholar] [CrossRef]
  56. Gautrat, P.; Laffont, C.; Frugier, F. Compact Root Architecture 2 Promotes Root Competence for Nodulation through the MiR2111 Systemic Effector. Curr. Biol. 2020, 30, 1339–1345. [Google Scholar] [CrossRef]
  57. Roy, S.; Müller, L.M. A Rulebook for Peptide Control of Legume-Microbe Endosymbioses. Trends Plant Sci 2022, 27, 870–889. [Google Scholar] [CrossRef]
  58. Breuillin, F.; Schramm, J.; Hajirezaei, M.; Ahkami, A.; Favre, P.; Druege, U.; Hause, B.; Bucher, M.; Kretzschmar, T.; Bossolini, E.; et al. Phosphate Systemically Inhibits Development of Arbuscular Mycorrhiza in Petunia hybrida and Represses Genes Involved in Mycorrhizal Functioning. Plant J. 2010, 64, 1002–1017. [Google Scholar] [CrossRef]
  59. Müller, L.M.; Harrison, M.J. Phytohormones, MiRNAs, and Peptide Signals Integrate Plant Phosphorus Status with Arbuscular Mycorrhizal Symbiosis. Curr. Opin. Plant Biol. 2019, 50, 132–139. [Google Scholar] [CrossRef]
  60. Meixner, C.; Ludwig-Müller, J.; Miersch, O.; Gresshoff, P.; Staehelin, C.; Vierheilig, H. Lack of Mycorrhizal Autoregulation and Phytohormonal Changes in the Supernodulating Soybean Mutant Nts1007. Planta 2005, 222, 709–715. [Google Scholar] [CrossRef]
  61. Wang, C.; Reid, J.B.; Foo, E. The Art of Self-Control—Autoregulation of Plant–Microbe Symbioses. Front. Plant Sci. 2018, 9, 988. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  62. Handa, Y.; Nishide, H.; Takeda, N.; Suzuki, Y.; Kawaguchi, M.; Saito, K. RNA-Seq Transcriptional Profiling of an Arbuscular Mycorrhiza Provides Insights into Regulated and Coordinated Gene Expression in Lotus japonicus and Rhizophagus irregularis. Plant Cell Physiol. 2015, 56, 1490–1511. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  63. van Zeijl, A.; Liu, W.; Xiao, T.T.; Kohlen, W.; Yang, W.-C.; Bisseling, T.; Geurts, R. The Strigolactone Biosynthesis Gene DWARF27 Is Co-Opted in Rhizobium Symbiosis. BMC Plant Biol. 2015, 15, 260. [Google Scholar] [CrossRef] [Green Version]
  64. Liang, G.; He, H.; Yu, D. Identification of Nitrogen Starvation-Responsive MicroRNAs in Arabidopsis Thaliana. PLoS ONE 2012, 7, e48951. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  65. Gifford, M.L.; Dean, A.; Gutierrez, R.A.; Coruzzi, G.M.; Birnbaum, K.D. Cell-Specific Nitrogen Responses Mediate Developmental Plasticity. Proc. Natl. Acad. Sci. USA 2008, 105, 803–808. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  66. Vidal, E.A.; Araus, V.; Lu, C.; Parry, G.; Green, P.J.; Coruzzi, G.M.; Gutiérrez, R.A. Nitrate-Responsive MiR393/AFB3 Regulatory Module Controls Root System Architecture in Arabidopsis Thaliana. Proc. Natl. Acad. Sci. USA 2010, 107, 4477–4482. [Google Scholar] [CrossRef] [Green Version]
  67. Zhao, M.; Ding, H.; Zhu, J.-K.; Zhang, F.; Li, W.-X. Involvement of MiR169 in the Nitrogen-Starvation Responses in Arabidopsis. New Phytol. 2011, 190, 906–915. [Google Scholar] [CrossRef] [Green Version]
  68. Fukuda, M.; Fujiwara, T.; Nishida, S. Roles of Non-Coding RNAs in Response to Nitrogen Availability in Plants. Int. J. Mol. Sci. 2020, 21, 8508. [Google Scholar] [CrossRef]
  69. Pant, B.D.; Buhtz, A.; Kehr, J.; Scheible, W.-R. MicroRNA399 Is a Long-Distance Signal for the Regulation of Plant Phosphate Homeostasis. Plant J. 2008, 53, 731–738. [Google Scholar] [CrossRef] [Green Version]
  70. Pant, B.D.; Musialak-Lange, M.; Nuc, P.; May, P.; Buhtz, A.; Kehr, J.; Walther, D.; Scheible, W.-R. Identification of Nutrient-Responsive Arabidopsis and Rapeseed MicroRNAs by Comprehensive Real-Time Polymerase Chain Reaction Profiling and Small RNA Sequencing. Plant Physiol. 2009, 150, 1541–1555. [Google Scholar] [CrossRef]
  71. Huen, A.; Bally, J.; Smith, P. Identification and Characterisation of MicroRNAs and Their Target Genes in Phosphate-Starved Nicotiana Benthamiana by Small RNA Deep Sequencing and 5′RACE Analysis. BMC Genom. 2018, 19, 940. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  72. Lin, S.-I.; Chiang, S.-F.; Lin, W.-Y.; Chen, J.-W.; Tseng, C.-Y.; Wu, P.-C.; Chiou, T.-J. Regulatory Network of MicroRNA399 and PHO2 by Systemic Signaling. Plant Physiol. 2008, 147, 732–746. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  73. Aung, K.; Lin, S.-I.; Wu, C.-C.; Huang, Y.-T.; Su, C.-L.; Chiou, T.-J. Pho2, a Phosphate Overaccumulator, Is Caused by a Nonsense Mutation in a MicroRNA399 Target Gene. Plant Physiol. 2006, 141, 1000–1011. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  74. Huang, T.-K.; Han, C.-L.; Lin, S.-I.; Chen, Y.-J.; Tsai, Y.-C.; Chen, Y.-R.; Chen, J.-W.; Lin, W.-Y.; Chen, P.-M.; Liu, T.-Y.; et al. Identification of Downstream Components of Ubiquitin-Conjugating Enzyme PHOSPHATE2 by Quantitative Membrane Proteomics in Arabidopsis Roots. Plant Cell 2013, 25, 4044–4060. [Google Scholar] [CrossRef] [Green Version]
  75. Branscheid, A.; Sieh, D.; Pant, B.D.; May, P.; Devers, E.A.; Elkrog, A.; Schauser, L.; Scheible, W.-R.; Krajinski, F. Expression Pattern Suggests a Role of MiR399 in the Regulation of the Cellular Response to Local Pi Increase during Arbuscular Mycorrhizal Symbiosis. Mol. Plant-Microbe Interact. 2010, 23, 915–926. [Google Scholar] [CrossRef] [Green Version]
  76. Etemadi, M.; Gutjahr, C.; Couzigou, J.-M.; Zouine, M.; Lauressergues, D.; Timmers, A.; Audran, C.; Bouzayen, M.; Bécard, G.; Combier, J.-P. Auxin Perception Is Required for Arbuscule Development in Arbuscular Mycorrhizal Symbiosis. Plant Physiol. 2014, 166, 281–292. [Google Scholar] [CrossRef] [Green Version]
  77. Couzigou, J.-M.; Lauressergues, D.; André, O.; Gutjahr, C.; Guillotin, B.; Bécard, G.; Combier, J.-P. Positive Gene Regulation by a Natural Protective MiRNA Enables Arbuscular Mycorrhizal Symbiosis. Cell Host Microbe 2017, 21, 106–112. [Google Scholar] [CrossRef] [Green Version]
  78. Lauressergues, D.; Delaux, P.-M.; Formey, D.; Lelandais-Brière, C.; Fort, S.; Cottaz, S.; Bécard, G.; Niebel, A.; Roux, C.; Combier, J.-P. The MicroRNA MiR171h Modulates Arbuscular Mycorrhizal Colonization of Medicago truncatula by Targeting NSP2. Plant J. 2012, 72, 512–522. [Google Scholar] [CrossRef]
  79. De Luis, A.; Markmann, K.; Cognat, V.; Holt, D.B.; Charpentier, M.; Parniske, M.; Stougaard, J.; Voinnet, O. Two MicroRNAs Linked to Nodule Infection and Nitrogen-Fixing Ability in the Legume Lotus japonicus. Plant Physiol. 2012, 160, 2137–2154. [Google Scholar] [CrossRef] [Green Version]
  80. Kaló, P.; Gleason, C.; Edwards, A.; Marsh, J.; Mitra, R.M.; Hirsch, S.; Jakab, J.; Sims, S.; Long, S.R.; Rogers, J.; et al. Nodulation Signaling in Legumes Requires NSP2, a Member of the GRAS Family of Transcriptional Regulators. Science 2005, 308, 1786–1789. [Google Scholar] [CrossRef]
  81. Heckmann, A.B.; Lombardo, F.; Miwa, H.; Perry, J.A.; Bunnewell, S.; Parniske, M.; Wang, T.L.; Downie, J.A. Lotus japonicus Nodulation Requires Two GRAS Domain Regulators, One of Which Is Functionally Conserved in a Non-Legume. Plant Physiol. 2006, 142, 1739–1750. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  82. Liu, W.; Kohlen, W.; Lillo, A.; Op den Camp, R.; Ivanov, S.; Hartog, M.; Limpens, E.; Jamil, M.; Smaczniak, C.; Kaufmann, K.; et al. Strigolactone Biosynthesis in Medicago truncatula and Rice Requires the Symbiotic GRAS-Type Transcription Factors NSP1 and NSP2. Plant Cell 2011, 23, 3853–3865. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  83. Hofferek, V.; Mendrinna, A.; Gaude, N.; Krajinski, F.; Devers, E.A. MiR171h Restricts Root Symbioses and Shows like Its Target NSP2 a Complex Transcriptional Regulation in Medicago truncatula. BMC Plant Biol. 2014, 14, 199. [Google Scholar] [CrossRef] [PubMed]
  84. Hoang, N.T.; Tóth, K.; Stacey, G. The Role of MicroRNAs in the Legume-Rhizobium Nitrogen-Fixing Symbiosis. J. Exp. Bot. 2020, 71, 1668–1680. [Google Scholar] [CrossRef] [PubMed]
  85. Yan, Z.; Hossain, M.S.; Arikit, S.; Valdés-López, O.; Zhai, J.; Wang, J.; Libault, M.; Ji, T.; Qiu, L.; Meyers, B.C.; et al. Identification of MicroRNAs and Their MRNA Targets during Soybean Nodule Development: Functional Analysis of the Role of MiR393j-3p in Soybean Nodulation. New Phytol. 2015, 207, 748–759. [Google Scholar] [CrossRef] [PubMed]
  86. Lelandais-Brière, C.; Naya, L.; Sallet, E.; Calenge, F.; Frugier, F.; Hartmann, C.; Gouzy, J.; Crespi, M. Genome-Wide Medicago truncatula Small RNA Analysis Revealed Novel MicroRNAs and Isoforms Differentially Regulated in Roots and Nodules. Plant Cell 2009, 21, 2780–2796. [Google Scholar] [CrossRef] [Green Version]
  87. Boualem, A.; Laporte, P.; Jovanovic, M.; Laffont, C.; Plet, J.; Combier, J.-P.; Niebel, A.; Crespi, M.; Frugier, F. MicroRNA166 Controls Root and Nodule Development in Medicago truncatula. Plant J. 2008, 54, 876–887. [Google Scholar] [CrossRef]
  88. Tsikou, D.; Yan, Z.; Holt, D.B.; Abel, N.B.; Reid, D.E.; Madsen, L.H.; Bhasin, H.; Sexauer, M.; Stougaard, J.; Markmann, K. Systemic Control of Legume Susceptibility to Rhizobial Infection by a Mobile MicroRNA. Science 2018, 362, 233–236. [Google Scholar] [CrossRef]
  89. Magori, S.; Oka-Kira, E.; Shibata, S.; Umehara, Y.; Kouchi, H.; Hase, Y.; Tanaka, A.; Sato, S.; Tabata, S.; Kawaguchi, M. Too Much Love, a Root Regulator Associated with the Long-Distance Control of Nodulation in Lotus japonicus. Mol. Plant-Microbe Interact. 2009, 22, 259–268. [Google Scholar] [CrossRef] [Green Version]
  90. Takahara, M.; Magori, S.; Soyano, T.; Okamoto, S.; Yoshida, C.; Yano, K.; Sato, S.; Tabata, S.; Yamaguchi, K.; Shigenobu, S.; et al. Too Much Love, a Novel Kelch Repeat-Containing F-Box Protein, Functions in the Long-Distance Regulation of the Legume–Rhizobium Symbiosis. Plant Cell Physiol. 2013, 54, 433–447. [Google Scholar] [CrossRef]
  91. Wang, Y.; Wang, L.; Zou, Y.; Chen, L.; Cai, Z.; Zhang, S.; Zhao, F.; Tian, Y.; Jiang, Q.; Ferguson, B.J.; et al. Soybean MiR172c Targets the Repressive AP2 Transcription Factor NNC1 to Activate ENOD40 Expression and Regulate Nodule Initiation. Plant Cell 2014, 26, 4782–4801. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  92. Wang, L.; Sun, Z.; Su, C.; Wang, Y.; Yan, Q.; Chen, J.; Ott, T.; Li, X. A GmNINa-MiR172c-NNC1 Regulatory Network Coordinates the Nodulation and Autoregulation of Nodulation Pathways in Soybean. Mol. Plant 2019, 12, 1211–1226. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  93. Holt, D.B.; Gupta, V.; Meyer, D.; Abel, N.B.; Andersen, S.U.; Stougaard, J.; Markmann, K. Micro RNA 172 (MiR172) Signals Epidermal Infection and Is Expressed in Cells Primed for Bacterial Invasion in Lotus japonicus Roots and Nodules. New Phytol. 2015, 208, 241–256. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  94. Yun, J.; Sun, Z.; Jiang, Q.; Wang, Y.; Wang, C.; Luo, Y.; Zhang, F.; Li, X. The MiR156b-GmSPL9d Module Modulates Nodulation by Targeting Multiple Core Nodulation Genes in Soybean. New Phytol. 2022, 233, 1881–1899. [Google Scholar] [CrossRef]
  95. Wang, Y.; Wang, Z.; Amyot, L.; Tian, L.; Xu, Z.; Gruber, M.Y.; Hannoufa, A. Ectopic Expression of MiR156 Represses Nodulation and Causes Morphological and Developmental Changes in Lotus japonicus. Mol. Genet. Genom. 2015, 290, 471–484. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  96. Okuma, N.; Soyano, T.; Suzaki, T.; Kawaguchi, M. MIR2111-5 Locus and Shoot-Accumulated Mature MiR2111 Systemically Enhance Nodulation Depending on HAR1 in Lotus japonicus. Nat. Commun. 2020, 11, 5192. [Google Scholar] [CrossRef]
  97. Skopelitis, D.S.; Hill, K.; Klesen, S.; Marco, C.F.; von Born, P.; Chitwood, D.H.; Timmermans, M.C.P. Gating of MiRNA Movement at Defined Cell-Cell Interfaces Governs Their Impact as Positional Signals. Nat. Commun. 2018, 9, 3107. [Google Scholar] [CrossRef]
  98. Jakobsen, I. The Role of Phosphorus in Nitrogen Fixation by Young Pea Plants (Pisum sativum). Physiol. Plant. 1985, 64, 190–196. [Google Scholar] [CrossRef]
  99. Kuang, R.-B.; Liao, H.; Yan, X.-L.; Dong, Y.-S. Phosphorus and Nitrogen Interactions in Field-Grown Soybean as Related to Genetic Attributes of Root Morphological and Nodular Traits. J. Integr. Plant Biol. 2005, 47, 549–559. [Google Scholar] [CrossRef]
  100. Divito, G.A.; Sadras, V.O. How Do Phosphorus, Potassium and Sulphur Affect Plant Growth and Biological Nitrogen Fixation in Crop and Pasture Legumes? A Meta-Analysis. Field Crops Res. 2014, 156, 161–171. [Google Scholar] [CrossRef]
  101. Gentili, F.; Huss-Danell, K. Local and Systemic Effects of Phosphorus and Nitrogen on Nodulation and Nodule Function in Alnus incana. J. Exp. Bot. 2003, 54, 2757–2767. [Google Scholar] [CrossRef] [PubMed]
  102. Isidra-Arellano, M.C.; Reyero-Saavedra, M.D.R.; Sánchez-Correa, M.D.S.; Pingault, L.; Sen, S.; Joshi, T.; Girard, L.; Castro-Guerrero, N.A.; Mendoza-Cozatl, D.G.; Libault, M.; et al. Phosphate Deficiency Negatively Affects Early Steps of the Symbiosis between Common Bean and Rhizobia. Genes 2018, 9, 498. [Google Scholar] [CrossRef] [PubMed]
Plants 12 00187 g001 550
Figure 1. Nutrient homeostasis and acquisition mechanisms involve regulation by peptide hormones and miRNAs. CLE and CEP peptides and miRNAs responding to (A) N availability, (B) rhizobia , (C) P availability and (D) arbuscular mycorrhizal fungi. Molecules that are induced or repressed by a respective stimulus are displayed in red or blue, respectively. Molecules that are responsive to more than one stimulus are in bold. Arrows indicate shoot-to-root or root-to-shoot translocation of mobile molecules. Specific responses are mediated by the shoot localized leucine-rich repeat receptor-like kinases HAR1/SUNN/NARK and CRA2/CEPR1. Lj, Lotus japonicus; Mt, Medicago truncatula; At, A. thaliana; Bn, Brassica napus; Gm, Glycine max; Pv, Phaseolus vulgaris; Sl, Solanum lycopersicum.
Figure 1. Nutrient homeostasis and acquisition mechanisms involve regulation by peptide hormones and miRNAs. CLE and CEP peptides and miRNAs responding to (A) N availability, (B) rhizobia , (C) P availability and (D) arbuscular mycorrhizal fungi. Molecules that are induced or repressed by a respective stimulus are displayed in red or blue, respectively. Molecules that are responsive to more than one stimulus are in bold. Arrows indicate shoot-to-root or root-to-shoot translocation of mobile molecules. Specific responses are mediated by the shoot localized leucine-rich repeat receptor-like kinases HAR1/SUNN/NARK and CRA2/CEPR1. Lj, Lotus japonicus; Mt, Medicago truncatula; At, A. thaliana; Bn, Brassica napus; Gm, Glycine max; Pv, Phaseolus vulgaris; Sl, Solanum lycopersicum.
Plants 12 00187 g001
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content.

Share and Cite

MDPI and ACS Style

Valmas, M.I.; Sexauer, M.; Markmann, K.; Tsikou, D. Plants Recruit Peptides and Micro RNAs to Regulate Nutrient Acquisition from Soil and Symbiosis. Plants 2023, 12, 187. https://doi.org/10.3390/plants12010187

AMA Style

Valmas MI, Sexauer M, Markmann K, Tsikou D. Plants Recruit Peptides and Micro RNAs to Regulate Nutrient Acquisition from Soil and Symbiosis. Plants. 2023; 12(1):187. https://doi.org/10.3390/plants12010187

Chicago/Turabian Style

Valmas, Marios I., Moritz Sexauer, Katharina Markmann, and Daniela Tsikou. 2023. "Plants Recruit Peptides and Micro RNAs to Regulate Nutrient Acquisition from Soil and Symbiosis" Plants 12, no. 1: 187. https://doi.org/10.3390/plants12010187

Note that from the first issue of 2016, this journal uses article numbers instead of page numbers. See further details here.

Article Metrics

Back to TopTop