Gene 865 (2023) 147328

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Review

Peptide signaling in anther development and pollen-stigma interactions

Tao Xiong a, Fan Ye b, Jiahui Chen b, Yurui Chen b, Zaibao Zhang a, *
a
College of Life Science, Xinyang Normal University, Xinyang, China
b
College of International Education, Xinyang Normal University, Xinyang, China

A R T I C L E I N F O A B S T R A C T

Edited by Tengbo Huang Polypeptides play irreplaceable roles in cell–cell communication by binding to receptor-like kinases. Various
types of peptide-receptor-like kinase-mediated signaling have been identified in anther development and mal­
Keywords: e–female interactions in flowering plants. Here, we provide a comprehensive summary of the biological functions
Peptide and signaling pathways of peptides and receptors involved in anther development, self-incompatibility, pollen
Receptor-like kinase
tube growth and pollen tube guidance.
Tapetum
Pollen-stigma interaction

1. Introduction
Cell-cell communications mediated through small molecule peptide
signals play essential roles in plant growth, development, fertilization
and stress responses. Plant small molecule peptides usually contain less
than 100 amino acids (Hsu and Benfey, 2018), and they can be divided
into two major types: post-translationally modified peptides and
cysteine-rich peptides (CRPs) (Matsubayashi, 2011). The post-
translationally modified peptides, composed of 5 to 20 amino acids in
length, are cleavage products of larger precursor proteins (Matsubaya­
shi, 2012). Cysteine-rich peptides (CRPs) usually comprise 40 to over
100 amino acids and contain multiple cysteine residues that form
intramolecular disulfide bonds. Both classes of peptides are secreted
extracellularly and recognized by membrane-associated receptor-like
kinases (RLKs), which activate signals that trigger many different
intracellular signaling. Plant genome contains many peptides and RLKs,
and more than 1000 peptides and 600 RLKs were identified in Arabi­
dopsis genome (Shiu and Bleecker, 2001; Lease and Walker, 2006). To
date, numerous peptides/RLK signaling have been identified and were
proved to play important roles in various developmental processes, such
as cell division, stem cell maintenance, anther development and pollen-
stigma interactions.
Anthers are the male organ of flowering plant where male gameto­
phytes (pollen) are produced. Anther contains multiple cell layers, and
the intercellular communications among different cell types are
important for anther development and pollen formation. Mature pollen
contains two sperm cells necessary for double fertilization with one
sperm cell fuses with the egg cell to form embryo and the other fuses
with central cell to produce endosperm. Double fertilization begins
when pollen reaches the stigma of the pistil. Then pollen absorbs water
from the stigma and the pollen tube germinates from the hydrated pollen
grain. The pollen tube grows in a directional polar pattern to through the

Abbreviations: CRPs, cysteine-rich peptides; RLKs, receptor-like kinases; TPD1, TAPETUM DETERMINANT 1; ScRALF3, Solanum chacoense Rapid Alkalinization
Factor 3; EMS1/EXS, EXCESS MICROSPOROCYTES 1/EXTRA SPOROGENOUS CELLS; LRR, leucine-rich repeat; SERK1, SOMATIC EMBRYO RECEPTOR KINASE 1;
BES1, BRI1 EMS SUPPRESSOR 1; BZR1, BRASSINAZOLE RESISTANT 1; SPL, SPOROCYTELESS; DYT1, DYSFUNCTIONAL TAPETUM 1; TDF1, TAPETUM DEVEL­
OPMENT AND FUNCTION 1; AMS, ABORTED MICROSPORES; MS1, MALE STERILITY 1; MSP1, MULTIPLE ARCHESPORIAL CELLS1; MAC1, MULTIPLE ARCHE­
SPORIAL CELL 1; AR, archesporial; CLE, CLAVATA3/EMBRYO SURROUNDING REGION (ESR)-RELATED; CIF3, CASPARIAN STRIP INTEGRITY FACTOR 3; GSO,
GASSHO; PCPs, POLLEN COAT PROTEINS; SI, self-incompatibility; SCR/SP11, S-LOCUS CYSTEINE RICH PROTEIN/S-LOCUS PROTEIN11; SRK, S-LOCUS RECEPTOR
KINASE; MLPKs, M− LOCUS PROTEIN KINASES; THL1 and THL2, THIOREDOXIN H-LIKE; ARC1, ARMADILLO-REPEAT-CONTAINING1; PLDα1, phospholipase D α-1
protein; GLO1, glyoxalase 1; SLR1-BP1 and SLR1-BP2, S locus-related glycoprotein 1 (SLR1)-binding proteins; SLR1, S-locus related 1; SLG, S-locus glycoprotein;
ANJ, ANJEA; FER, FERONIA; CrRLK1L, Catharanthus roseus receptor-like kinase 1-like; RALF23/33, RAPID ALKALINAZATION FACTOR23/33; ROS, reactive oxygen
species; LAT52, LATE ANTHER TOMATO52; LePRK2, POLLEN-SPECIFIC RECEPTOR KINASE2; LeSTIG1, STIGMA-SPECIFIC PROTEIN1; SCA, STIGMA/STYLE
CYSTEINE-RICH ADHESIN; TTE, TT epidermis; RALF, RAPID ALKALIZATION FACTOR; BUPS1, BUDDA’S PAPER SEAL1; ANX1, ANXUR1; PMCs, pollen mother cells;
MEL2, MEIOSIS ARRESTED AT LEPTOTENE2; LEPTO1, LEPTOTENE 1; JA, jasmonic acid.
* Corresponding author.
E-mail address: zaibaozhang79@163.com (Z. Zhang).

https://doi.org/10.1016/j.gene.2023.147328
Received 24 November 2022; Received in revised form 25 January 2023; Accepted 27 February 2023
Available online 2 March 2023
0378-1119/© 2023 Elsevier B.V. All rights reserved.
T. Xiong et al. Gene 865 (2023) 147328

Table 1
Peptide signaling in anther development and pollen-stigma interactions.
Peptide Genus Expression site Receptors Signaling components Functions Reference
name

TPD1 Arabidopsis microsporocyts and EMS1 BES1 Formation and development of tapetum (Chen et al.,
thaliana tapetum 2019)
OsTDL1A Oryza sativa tapetum MSP1 n.d. Formation and development of tapetum (Yang et al.,
and middle layer 2016)
MAC1 Zea mays archesporial ZmMSP1 n.d. Inhibition of archesporial cell proliferation (Wang et al.,
cells 2012)
CLE19 Arabidopsis tapetum RLKs* AMS,MS188,MS1 Extine development (Wang et al.,
thaliana 2017b)
CIF3/CIF4 Arabidopsis tapetum GSO1/GSO2 SBT5.4 Pollen wall formation (Truskina et al.,
thaliana 2022)
SCR/SP11 Brassica napus tapetum and pollen SRK ARC1, THL1/2 Self-incompatibility (Shiba et al.,
2001)
PCP-A1 Brassica napus developing pollen SLG n.d. Self-incompatibility (Takayama et al.,
2000)
PCP-Bs Arabidopsis developing pollen ANJ-FER ROS Promotes pollen adhesion, hydration, (Wang et al.,
thaliana and tube growth 2017a)
RALF23/33 Arabidopsis stigma ANJ-FER ROS Initiating pollen hydration (Stegmann et al.,
thaliana 2017)
LeLAT52 Lycopersicon pollen LePRK2 n.d. Pollen hydration and germination （Twell et al.,
esculentum 1989）
LeSTIG1 Lycopersicon stigma LePRK1, KPP Pollen germination and tube growth (Huang et al.,
esculentum LePRK2 2014)
SCA Lilium longiflorum stylar TT epidermis n.d. n.d. Pollen tube adhesion (Kim et al., 2003)
TfLURE1/ Torenia fournieri synergid cells n.d. n.d. Pollen tube guidance and attraction (Okuda et al.,
TfLURE2 2009)
AtLURE1s Arabidopsis synergid cells PRK6, MDIS- ROP1 micropylar pollen tube guidance, Species- (Zhong et al.,
thaliana MIK specific pollen tube attraction 2019)
XIUQIUs Brassicaceae synergid cells PRK6 n.d. general pollen tube attraction (Zhong et al.,
2019)
RALF4/19 Arabidopsis n.d. BUPS1/2, MRI, AUN1/2, RbohH and Pollen tube integrity (Ge et al., 2019)
thaliana ANX1/2 RbohJ NADPH oxidases
RALF34 Arabidopsis n.d. ANX1/2, n.d. Pollen tube rupture and sperm release (Ge et al., 2019)
thaliana BUPS1/2

Notes to Table 1: n.d., no data; * Receptor for prediction.

stigma and reach the ovary. Finally, the two sperm cells were released
from the pollen tube and finished the fertilization process by fuses with
the egg cell and the central cell, respectively. In all of these processes,
without exception, the peptide/RLK signaling plays vital roles. In this
review, we mainly summarized the role of various peptide/RLK
signaling in anther development and in pollen-stigma interactions that
have broadened our knowledge about sexual reproduction in flowering
plants.
2. The TPD1-EMS1 signal determines tapetum differentiation
Anthers are the male parts of flowers and a mature anther contains
four somatic cell layers (epidermis, endothecium, middle layer and
tapetum, listed from outside to inside) and one reproductive cell layer
(microsporocytes). Microsporocytes produce pollen via meiosis, and the
somatic cells, particularly the tapetum, are essential for normal devel­
opment and the release of pollen. Most anther cells (endothecium,
middle layer, tapetum and microsporocyte) originate from the same
Layer 2 cells, thus anther development involves numerous cell division
and cell differentiation. The signal transduction of small peptides is
shown in all aspects of plant reproduction, such as Solanum chacoense
Rapid Alkalinization Factor 3 (ScRALF3) participates in the signal
transmission from sporophyte to gametophyte and affects pollen mitosis
I (Loubert-Hudon et al., 2020). Therefore, the intracellular communi­
cations among somatic and reproductive cells are essential for cell fate
determination, and many peptide/RLK signaling have been proved to
play key roles in regulating cell–cell communications in Arabidopsis,
rice and maize anthers (Table 1). In addition, some peptides, such as
BnaC.SP6, are small secretory peptides expressed in mature anthers and
pod membranes, which are essential for the maintenance of pollen ac­
tivity (Wang et al., 2017c).
Arabidopsis TAPETUM DETERMINANT 1 (TPD1) encodes a small
secreted cysteine-rich peptide. It is expressed in both developing mi­
crosporocytes and tapetum, with a higher expression was detected in
microsporocytes than that in tapetum (Yang et al., 2003). The TPD1
mutation affects the development of tapetum and its mutant displayed
extra microsporocytes and absence of tapetum phenotype (Yang et al.,
2003). Both overexpression and ectopic expression of TPD1 affect
tapetum determination and inhibit microsporocyte development, indi­
cating that TPD1 plays an essential role in the differentiation of tapetum
(Yang et al., 2005; Jia et al., 2008).
TPD1 is secreted to extracellular space and function as a ligand for
EXCESS MICROSPOROCYTES 1/EXTRA SPOROGENOUS CELLS (EMS1/
EXS) (Yang et al., 2005). EMS1 encodes a leucine-rich repeat (LRR)
receptor-like kinase (LRR-RLK), and displays a specially expression in
tapetum (Zhao et al., 2002; Huang et al., 2016). The ems1 sterile
phenotype is similar to that of tpd1 mutant, with no tapetum layer was
formed in ems1 mutant. The TPD1 peptide is restricted to microsporo­
cytes, while the EMS1 protein is restricted to tapetum (Huang et al.,
2016). TPD1 interacts with the extracellular LRR region of EMS1, and
induces EMS1 phosphorylation (Fig. 1) (Jia et al., 2008). Genetic ana­
lyses show that two LRR-RLKs, SOMATIC EMBRYO RECEPTOR KINASE
1 (SERK1) and SERK2 function in the same signaling pathway as EMS1,
for the serk1serk2 double mutants display a sterile phenotype same as
that of ems1 and tpd1 mutants. SERK1 and SERK2 display an overlap
expression with EMS1, with more transcripts were identified in tapetum
(Albrecht et al., 2005; Colcombet et al., 2005). SERK1 and SERK2
interact with EMS1 in vivo and function as the coreceptor of EMS1 (Chen
et al., 2019). In the presence of TPD1, SERK1/2 and EMS1 assemble a
stable heterodimer, which leads to transphosphorylation between
SERK1/2 and EMS1. The BRI1 EMS SUPPRESSOR 1 (BES1) and BRAS­
SINAZOLE RESISTANT 1 (BZR1) transcription factors function as
downstream targets of the TPD1-EMS-SERK1/2 pathway. Both BES1 and
BZR1 are expressed in tapetum and the quintuple mutant of BES1 family

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T. Xiong et al. Gene 865 (2023) 147328

Fig. 1. The role of small molecular peptides in anther development. Mutant phenotypes (A), Signal transduction pathways of small peptides and their cognate
receptors expressed in the tapetum layer (B), and model diagram of pollen wall formation coordinated with tapetum layer development (C). In the A-plot, the tpd1/
ems1/serk1/2 mutants are highly similar in phenotype, showing additional microspore mother cells and absence of the tapetum layer, and the msp1/ostdl1a mutants
are similar in phenotype, showing absence of the middle layer and tapetum layer. In the B-plot, TPD1 binds to EMS1, and SERK1/2 functions as a co-receptor for
EMS1 to phosphorylate the downstream gene BES1, which subsequently binds to the promoter regions of genes related to tapetum development, such as SPL, DYT1,
and TDF1, regulating formation and development of the tapetum layer. MSP1 is co-expressed with OsTDL1A in the tapetum layer and limits the number of spor­
ocytes, and its downstream genes are not known. CLE19 is may bind to RLKs to negatively regulate the AMS-MYB103-MS1 transcriptional cascade, preventing its
deleterious overexpression and contributing to the normal expression of genes related to downstream outer wall formation, secretion of sporopollenin, and pollen
outer wall formation. In the C-plot, the CIF3/CIF4 precursor produced by the tapetum layer is first sheared at the plasma membrane by SBT5.4 from pollen. Activated
CIF3/CIF4 diffuses to the middle layer and binds to GSO1/GSO2 on the plasma membrane of the middle layer to transmit the signal into the middle layer. Then the
middle layer sends the signal back to the tapetum, which secretes sporopollen to the pollen surface and promotes the formation of pollen exine. Abbreviations: E,
epidermis; En, endothecium; ML, middle layer; T, tapetum; eMC, extra microsporocytes; Sp, sporogenous cell; UIC, unknown identity cell; eSp, excessive sporog­
enous cell.

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T. Xiong et al. Gene 865 (2023) 147328

Fig. 2. The role of peptides in self-incompatibility and pollen hydration. (A) SCR/SP11 is secreted to the pollen surface to bind to SRK located in the stigma.
MLPKs is the coreceptor of SRK. THL1 and THL2 interact with SRK and negatively regulate self-incompatibility, thus activating its downstream gene ARC1. PCP-A1 is
secreted to the pollen surface and binds to SLG to mediate self-incompatibility, but its downstream signal is not clear. (B) During pollination, PCP-B competes with
RALF23/33 to bind ANJ-FER, thus inhibiting the production of ROS and initiating pollen hydration on the stigma.

(bes1 bzr1 beh1 beh3 beh4) displays a tapetum absent phenotype, similar
to the phenotype in ems1, tpd1 and serk1serk2 mutants. In anther, the
BES1 is phosphorylated and transported into nuclear, where it directly
binds and regulates the expression of many essential tapetum develop­
mental genes, including SPOROCYTELESS (SPL), DYSFUNCTIONAL
TAPETUM 1 (DYT1), and TAPETUM DEVELOPMENT AND FUNCTION 1
(TDF1), ABORTED MICROSPORES (AMS), MALE STERILITY 1 (MS1),
and MS2 (Fig. 1) (Chen et al., 2019). Therefore, the TPD1-EMS1-SERK1/
2-BES1 signaling play essential roles in tapetum differentiation.
The TPD1-EMS1 mediated signaling is observed in rice and maize. In
rice, the EMS1 ortholog and the TPD1 ortholog, MULTIPLE ARCHE­
SPORIAL CELLS1 (MSP1) and TDL1A, have been identified, respectively
(Fig. 1, Table 1) (Nonomura et al., 2003; Zhao et al., 2008). Disruption
of MSP1 and TDL1A cause similar anther defects phenotypes to that of
ems1 and tpd1 mutants. TDL1A binds to the LRR domain of MSP1, and
TDL1A-MSP1 signaling promotes the development of parietal cells into
the middle layer and tapetal layer (Yang et al., 2016). These results
indicate that the function of TPD1-EMS1 signaling is conserved in anther
cell differentiation between dicots and monocots. However, many
expression and phenotypic differences between rice and Arabidopsis
orthologs and mutants were identified. TDL1A and MSP1 are also
expressed in ovules and both tdl1a and msp1 mutants affect the ovule
development. These distinctions reflect the species-specific character­
istics of TPD1-EMS1 signaling pathway. In addition, MSP1 is also
involved in the differentiation of sporogenous cells, meiosis and the
development of pollen mother cells (PMCs) (Zhao et al., 2021). MEIOSIS
ARRESTED AT LEPTOTENE 2 (MEL2) and LEPTOTENE 1 (LEPTO1) are
two key regulators involved in the process of meiosis in rice. Their de­
letions lead to chromosome defects in the leptotene (Zhao et al., 2018).
LEPTO1 and MEL2 are involved in the establishment of leptotene
chromosomes, and function downstream of MSP1 and its ligand MIL2/
OsTDL1A (Hong et al., 2012; Zhao et al., 2021).
MULTIPLE ARCHESPORIAL CELL 1 (MAC1) is the ortholog of TPD1
in maize (Wang et al., 2012). Mutation of MAC1 leads to the absence of
the tapetum and increased archesporial (AR) cells in anther, identical to
the phenotype of msp1. Therefore, MAC1 inhibits excessive proliferation
of archesporial (AR) cells and promotes periclinal division of subepi­
dermal cells at an early stage of anther development (Wang et al., 2012).
MAC1 binds the ZmMSP1 (van der Linde et al., 2018), an ortholog of rice
MSP1, but the downstream signaling is still not clear.
3. Peptide signaling during pollen wall development
Pollen is the male gametophyte of higher plants, and is essential for
sexual reproduction. Pollen is protected by pollen wall, which plays
essential roles in protecting male gametophytes against to various biotic
and abiotic stresses, pollen-stigma communication and fertilization
(Jiang et al., 2013). In higher plants, pollen wall is composed of intine,
exine and pollen coat, and tapetum plays important roles in the for­
mation of exine and pollen coat. The main component of exine is
sporopollenin, which is synthesized in tapetum and polarized transport
to pollen surface. Many peptide genes are expressed in tapetum and

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T. Xiong et al.
involved in pollen wall development.
CLAVATA3/EMBRYO SURROUNDING REGION (ESR)-RELATED
(CLE) genes encode peptide ligands and play important roles in various
plant developmental processes. For instance, CLV3 and CLE40 play
essential roles in stem cell maintenance in shoot apical meristem and
root apical meristem, respectively (Fletcher et al., 1999; Stahl and
Simon, 2009). 32 CLE genes are identified in Arabidopsis genome and 7
CLE (CLE9, CLE16, CLE17, CLE19, CLE41, CLE42 and CLE45) genes are
expressed in tapetum (Cock and McCormick, 2001; Wang et al., 2017b).
Both dominant-negative (DN) and overexpression (OX) of the CLE19
gene showed obviously male fertility defects. Pollen exine formation is
affected in cle19 mutants, and the expression of many tapetum tran­
scription factor genes (eg. AMS, MS188, MS1) is upregulated in DN-
CLE19 and CLE19-OX anthers, indicating that CLE19 functions as a
negative regulator in pollen wall development (Fig. 1, Table 1). The
receptors for perceiving the CLE19 is not clear. Many RLK genes are
expressed in tapetum and may function as the CLE19 receptor which
needs to be investigated in the future.
Although tapetum plays essential roles in pollen wall development,
the regulation mechanism of tapetum activity is still not clearly under­
stood. Recently, Truskina et al reported a complex peptide/RLK
signaling spanning middle layer, tapetum and pollen is necessary for the
coordination of tapetum activity with pollen development (Fig. 1,
Table 1) (Truskina et al., 2022). They found that CASPARIAN STRIP
INTEGRITY FACTOR 3 (CIF3) and CIF4 regulate tapetum activity by
binding to the GASSHO (GSO) receptor-like kinase (GSO1 and GSO2).
GSO1 and GSO2 are produced in the middle layer, while CIF3 and CIF4
are expressed in the tapetum cells. gso1 gso2 and cif3 cif4 double mutants
display similar phenotype with swollen tapetum and abnormal deposi­
tion of pollen wall. CIF3 and CIF4 belong to sulfo-peptides and its pre­
cursors need posttranslational tyrosine sulfation for GSO binding and
activity. SBT5.4, a pollen expressed subtilisin serine protease, is required
for the activation of CIF3 and CIF4 peptides by cleaving the C-terminal
extension of CIF precursors. Therefore, a hypothesis model for the co­
ordination between pollen wall formation with tapetum activity was
developed (Fig. 1) (Truskina et al., 2022). The tapetum expressed CIF
precursors are processed by the pollen-derived SBT5.4, then the acti­
vated CIF peptides diffuse to bind GSO receptors in the middle layer,
which regulate the polarize secretion of sporopollenin from the tapetum.
How the middle layer expressed GSO1 and GSO2 affect the polarization
of tapetum needs to be further investigated.
4. PCP peptides involved in pollen recognition and pollen
hydration
The interaction between pollen and stigma is the prerequisite for
double fertilization. Pollen-stigma interactions begin with the adhesion
of mature pollen to the stigma, followed by pollen hydration that causes
the pollen tube to germinate until the pollen tube grows in a directional
polar pattern to reach the embryo sac. Pollen adhesion depends on the
interactions between the outer wall of the pollen and the stigma, and the
hydration of pollen on the stigma is essential for successful pollination of
the plant and facilitates the process of pollen tube germination, where
the pollen tube reaches the synergid cell to rupture to release two sperm
and begin double fertilization.
The pollen coat is the outermost stratum of the pollen surface. It is
mainly composed of lipids, proteins, carotenoids, flavonoids, and car­
bohydrates that are mainly produced in tapetum (Mayfield et al., 2001;
Rejón et al., 2016). Many kinds of POLLEN COAT PROTEINS (PCPs)
were identified in pollen coat and mediated self-incompatibility (SI) by
function as receptor peptides. In Brassicaceae, a number of CRP peptides
were identified and function in SI. In Brassica napus, S-LOCUS CYSTEINE
RICH PROTEIN/S-LOCUS PROTEIN11 (SCR/SP11), the male de­
terminants of SI, is expressed in tapetum and pollen, and is further
coated the pollen surface (Fig. 2, Table 1) (Shiba et al., 2001). During the
early stage of pollen-stigma interactions, the SCR/SP11 peptides are
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Gene 865 (2023) 147328
secreted form the pollen coat and recognized by the papilla cell
expressed S-LOCUS RECEPTOR KINASE (SRK) (Silva et al., 2001). M-
LOCUS PROTEIN KINASES (MLPKs), function as the coreceptor of SRK,
play positive roles in SI (Murase et al., 2004). THIOREDOXIN H-LIKE
proteins (THL1 and THL2) function as negative regulators of SI, inter­
acting with SRK and inhibiting its kinase activity (Bower et al., 1996;
Haffani et al., 2004). The interaction of SCR/SP11-SRK releases the
THL1/THL2 from the complex and activates the downstream gene
ARMADILLO-REPEAT-CONTAINING1 (ARC1) (Stone et al., 2003; Haf­
fani et al., 2004). ARC1 encodes a E3 ubiquitin ligase and mediates
ubiquitination and proteasomal degradation of many downstream pro­
teins, such as Exo70A1, phospholipase D α-1 protein (PLDα1), glyox­
alase 1 (GLO1), which inhibit pollen hydration and pollen germination
of the self-pollen on the stigma (Stone et al., 2003; Sankaranarayanan
et al., 2015; Scandola and Samuel, 2019; Kim et al., 2021) (Fig. 2). Other
pollen expressed CRPs that belong to the PCP-A class are also function in
SI responses in Brassica. Two S locus-related glycoprotein 1 (SLR1)-
binding proteins (SLR1-BP1 and SLR1-BP2) and one PCP-A1 peptide are
deposited in pollen coat and bind the stigmatic proteins S-locus related 1
(SLR1) and S-locus glycoprotein (SLG), respectively (Fig. 2, Table 1)
(Doughty et al., 1998; Takayama et al., 2000). The downstream signal of
PCP-A1/SLG in unknown (Fig. 2).
Arabidopsis is a self-compatible plant, and four pollen-expressed
PCP-B peptides (AtPCP-Bα, AtPCP-Bβ, AtPCP-Bγ, AtPCP-Bδ) were re­
ported to mediate self-compatible responses (Fig. 2, Table 1). Mutations
in pcp-bα/β/γ impaired pollen adhesion, reduced hydration rate, and
delayed pollen tube growth in vivo (Wang et al., 2017a). The PCP-B
proteins, belonging to the CRP class, are expressed in developing pol­
len and secreted to the pollen coat (Fig. 2). They played a regulatory role
in the early stages of pollen-stigma interaction that functioned as an
early checkpoint for affinity hydration (Wang et al., 2017a). ANJEA
(ANJ) and FERONIA (FER) are members of the Catharanthus roseus
receptor-like kinase 1-like (CrRLK1L) gene family (Li et al., 2016). ANJ
and FER are expressed in the papilla cell of stigma, and the single anj and
fer mutants and the double anj fer mutants promote pollen hydration
(Liu et al., 2021). Before pollination, the ANF-FER receptors bind the
autocrine peptides RAPID ALKALINAZATION FACTOR23/33 (RALF23/
33) (Haruta et al., 2014; Ge et al., 2017; Stegmann et al., 2017), and
induce high reactive oxygen species (ROS) production in papilla cell by
activating the expression of NADPH oxidase RBOHD (Liu et al., 2021).
During pollination, PCP-Bs compete with RALF23/33 to bind the ANJ-
FER, thereby repressing ROS production and initiating pollen hydra­
tion on stigma (Fig. 2) (Liu et al., 2021).
5. Peptides involved in pollen tube growth, guidance and
reception
Pollen germination occurs after the completion of pollen hydration.
The pollen tubes grow polarly in the transmitting tract to the ovary
(pollen tube guidance) and rupture in the embryo sac (pollen tube
reception) to release the two sperm cells for double fertilization. Many
peptide/RLK-mediated pollen tube guidance and reception have been
well summarized (Higashiyama, 2010; Zhong and Qu, 2019; Hafidh and
Honys, 2021; Kim et al., 2021). For example, before pollen germination,
the tomato pollen autocrine peptide LATE ANTHER TOMATO52
(LAT52) interacts with the POLLEN-SPECIFIC RECEPTOR KINASE2
(LePRK2), which promotes pollen hydration and germination (Table 1)
(Twell et al., 1989; Muschietti et al., 1994). After pollen germination,
another stigma CRP peptide STIGMA-SPECIFIC PROTEIN1 (LeSTIG1) is
expressed and competes with LAT52 to form LeSTIG1-LePRK2 complex
to promote pollen tube growth (Tang et al., 2002; Tang et al., 2004;
Huang et al., 2014). Therefore, LePRK2 switches its partner from LAT52
to LeSTIG1 during pollen germination and pollen tube growth.
During pollen tube growth, various female-secreted peptides
mediate pollen tube guidance and pollen tube reception (Table 1). Lilium
longiflorum STIGMA/STYLE CYSTEINE-RICH ADHESIN (SCA) peptide, a
T. Xiong et al. Gene 865 (2023) 147328

Fig. 3. Peptide genic male sterility system for hybrid production. The plants of male sterile lines were sprayed with polypeptide hormones and the fertility of
their offspring was restored.

6
T. Xiong et al.
CRP peptide secreted from the stylar TT epidermis (TTE), mediates the
pollen tube tip growth by promoting the adhesion of pollen tubes to the
stylar TTE (Mollet et al., 2000; Kim et al., 2003). In Torenia fournieri,
LURE1 and LURE3, members of CRPs, are specifically localized in syn­
ergid cells and function as pollen tube attractants (Table 1) (Okuda
et al., 2009). The Arabidopsis LURE homologs (AtLURE1s) were iden­
tified and showed strong pollen tube attraction activity (Okuda et al.,
2009). Two pollen tube-localized LRR-RLKs, PRK6 and the MDIS-MIK
complex, are receptors of AtLURE1s and mediate micropylar pollen
tube guidance (Table 1) (Zhong et al., 2019). The AtLRUE1-related
XIUQIUs are also specifically expressed in synergid cells and function
as general pollen tube attractants independently of the PRK6 receptor
(Zhong et al., 2019). Therefore, the XIUQIU peptides can be used in
interspecific fertilization in future plant breeding.
After arrival of the pollen tube at the embryo sac, it enters one of two
synergid cells, stops growing and bursts to release two sperm cells for
fertilization. These biological processes are strictly controlled by pep­
tide/RLK signaling between the pollen tube and the synergid cell (Kim
et al., 2021). The synergid cell expressed LRR-RLK, FERONIA (FER)/
SIRENE, mediates pollen tube cessation and rupture, for the fer mutant
pollen continues to grow and does not burst (Table 1) (Wolf and Hofte,
2014). The FER receptor is also involved in regulation of root growth
and the immune responses by interacting with the RAPID ALKALIZA­
TION FACTOR (RALF) peptide, RALF1 and RALF23, respectively (Wolf
and Hofte, 2014). The pollen tube secreted RALF ligands for FER have
not yet been identified. In addition, two FER homologs, BUDDA’S
PAPER SEAL1 (BUPS1) and BUPS2, form a complex with two LRR-RLKs,
ANXUR1 (ANX1) and ANX2, in pollen tubes to regulate pollen tube
integrity (Ge et al., 2019). Both double mutants of bups1 bups2 and anx1
anx2 cause precocious rupture of pollen tube (Ge et al., 2019). Two
pollen tube-expressed RALF peptides, RALF4 and RALF19, function as
the ligands of BUPS/ANX receptor complex(Ge et al., 2019). Interest­
ingly, the female-derived peptide, RALF34, can compete with RALF4/19
to bind BUPS/ANX complex and induce pollen tube rupture and sperm
release (Ge et al., 2019). Therefore, both autocrine and paracrine signal
RALF-BUPS/ANX complexes control pollen tube integrity and rupture.
6. Developing male sterile mutants for hybrid breeding
Male sterile plants are the fundamental breeding materials, and the
identified and characterized genic male sterility genes are exploited for
hybrid breeding. For example, a male sterile mutant osopr7, which
created with CRISPR/Cas9 system, was used for hybrid production (Pak
et al., 2021). OsOPR7 encodes a 12-oxophytodienoate reductase, which
is a precursor for the biosynthesis of jasmonic acid (JA). Moreover,
exogeneous application of MeJA can rescue the fertile phenotype and
facilitate hybrid production. Hence, this system can also be used in
peptide genes and applied to the production of hybrid crops in the future
(Fig. 3).
7. Concluding remarks and perspectives
In higher plants, anther development and pollen-stigma interaction
require complex cell–cell communications, and various peptide/RLK
signaling play essential roles in these processes. In this review, we
provide a comprehensive summary and overview of the role of peptide/
RLK signaling during anther development and subsequent pollen-stigma
interactions. However, the function and regulatory mechanisms of many
peptide/RLKs are still not clear. The mitogen activated protein kinase
(MAPK) cascade was demonstrated function downstream of many pep­
tide/RLK signaling. Further studies need to identify the MAPK compo­
nents and the molecules that linking peptide/RLK with the downstream
MAPK cascade. The plant genome contains a huge number of peptides
and RLKs, and these peptide/RLK genes have high genetic redundancy.
Therefore, new genome editing technologies, including CRISPR-Cas9,
are useful to investigate the biological functions of these redundant
7
Gene 865 (2023) 147328
peptide/RLK genes. With further research, it is expected that more and
more peptide/RLK signaling will be explored, which improve our un­
derstanding of peptide/RLK signaling in anther development and sexual
reproduction.
Funding information
This work has been supported by the National Natural Science
Foundation of China (32170351) and Nanhu Scholars Program for
Young Scholars of Xinyang Normal University.
Data Availability
No data was used for the research described in the article.
Declaration of Competing Interest
The authors declare that they have no known competing financial
interests or personal relationships that could have appeared to influence
the work reported in this paper.
Data availability
No data was used for the research described in the article.
Acknowledgements
The authors would like special thanks to the reviewers for their
helpful and constructive suggestions and comment to improve the
quality of the paper.
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