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Pollen-Pistil Interaction

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A special issue of International Journal of Molecular Sciences (ISSN 1422-0067). This special issue belongs to the section "Molecular Plant Sciences".

Deadline for manuscript submissions: closed (30 June 2022) | Viewed by 28332

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Prof. Dr. Stefano Del Duca

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Guest Editor

Department of Biology, Alma Mater Studiorum University of Bologna, Bologna, Italy
Interests: plant reproduction; pollen tube growth; self-incompatibility; programmed cell death; pollen allergens
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Dr. Giampiero Cai

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Guest Editor

Department of Life Sciences, University of Siena, Siena, Italy
Interests: cytoskeleton; cell wall; organelle movement; cell morphogenesis; plant reproduction; abiotic stress
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Dr. Iris Aloisi

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Guest Editor

Department of Biological, Geological, and Environmental Sciences, University of Bologna, Bologna, Italy
Interests: pollen morphology; pollen transglutaminase; self-incompatibility response; polyamines
Special Issues, Collections and Topics in MDPI journals

Special Issue Information

Dear Colleagues,

Pollen and the pollen tube are fundamental cell systems in the life of seed plants, as they are used to transport male gametes to promote sexual reproduction. In addition to being a biological system of fundamental importance to plant life, pollen and pollen tubes have been considered an excellent study model for several years. Although they are not photosynthetic cells, pollen tubes contain all the typical components of a plant cell organized along a temporal developmental axis (once called “zonation”). This prerogative, which pollen tubes share with root hair cells, makes the male gametophyte a very useful system for studying many processes that occur in plant cells. From a biological perspective, the pollen tube is successful in fertilization because of a network of interactions that is only beginning to be fully understood in recent years. Fundamentally, the pistil produces a series of chemically distinct signaling molecules that must be intercepted by receptors in the pollen tube plasma membrane, especially in its apical region. From the receptors, information must be transduced by a set of intracellular messengers that include proteins, ion flux, and other molecules. This integrated system of messengers is used to modulate the activity of the pollen tube cytoskeleton and thus the flux of organelles and vesicles; the interaction between the transduction systems and cytoskeleton activity modulates cell wall integrity and thus pollen tube growth. At the same time, the pollen tube secretes signals perceived by pistil cells, thus contributing to a continuous crosstalk. The dialogue between pistil and pollen tube is more complex in self-incompatible species, which can reject the incompatible pollen tube, thus promoting genetic variability. Self-incompatibility is complex and characterized by specific proteins that must, however, interface with the signal transduction system and cytoskeleton.

The impact that climate change can have on the molecular dialogue between pistil and pollen tube should not be omitted or even underestimated. What we now call environmental stress (i.e., changes in temperature, water availability, salinity, etc.) can affect one or more steps in the dialogue between pistil and pollen grain and/or tube leading to missed or undesired plant fertilization and reproduction. It should not be forgotten that some proteins released from pollen grains and pollen tubes are allergens that, under conditions of climate change, could be present at higher levels and sensitizing capacity, thus increasing health problems.

This Special Issue aims to collect contributions, both as original articles and reviews, on the molecular dialogue between pollen tube and pistil. Topics such as regulation of pollen tube growth, the role of miRNAs, extracellular signals from pistil (peptides, hormones, lipid-binding proteins), peptides secreted by pollen tube, nanovesicles, the role of AGPs, transduction factors (receptors, ROS, Ca2+, proton pumps, etc.), cell wall integrity, the role of cytoskeleton, environmental stress, and incompatibility, are all welcome. We emphasize the importance of studying the interplay between the above topics, especially from the perspective of self-incompatibility and environmental conditions that could affect the information network, causing either failure or incorrect success of plant reproduction. If studies focus on plants of economic interest, these issues will have a significant impact in agriculture.

Prof. Dr. Stefano Del Duca
Dr. Giampiero Cai
Dr. Iris Aloisi
Guest Editors

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Published Papers (12 papers)

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Editorial

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4 pages, 201 KiB

Open AccessEditorial

Pollen-Pistil Interaction

by Giampiero Cai, Iris Aloisi and Stefano Del Duca

Int. J. Mol. Sci. 2023, 24(4), 3707; https://0-doi-org.brum.beds.ac.uk/10.3390/ijms24043707 - 13 Feb 2023

Viewed by 1511

Abstract

The aim of this Special Issue is to highlight the molecular dialogue between the pollen tube and the pistil [...] Full article

(This article belongs to the Special Issue Pollen-Pistil Interaction)

Research

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17 pages, 3558 KiB

Open AccessArticle

Expression of Clementine Asp-Rich Proteins (CcASP-RICH) in Tobacco Plants Interferes with the Mechanism of Pollen Tube Growth

by Luigi Parrotta, Lavinia Mareri, Iris Aloisi, Claudia Faleri, Gaetano Distefano, Alessandra Gentile, Angela Roberta Lo Piero, Verena Kriechbaumer, Marco Caruso, Giampiero Cai and Stefano Del Duca

Int. J. Mol. Sci. 2022, 23(14), 7880; https://0-doi-org.brum.beds.ac.uk/10.3390/ijms23147880 - 17 Jul 2022

Cited by 2 | Viewed by 1865

Abstract

Low-molecular-weight, aspartic-acid-rich proteins (ASP-RICH) have been assumed to be involved in the self-incompatibility process of clementine. The role of ASP-RICH is not known, but hypothetically they could sequester calcium ions (Ca²⁺) and affect Ca²⁺-dependent mechanisms. In this article, we analyzed the effects induced by clementine ASP-RICH proteins (CcASP-RICH) when expressed in the tobacco heterologous system, focusing on the male gametophyte. The aim was to gain insight into the mechanism of action of ASP-RICH in a well-known cellular system, i.e., the pollen tube. Pollen tubes of tobacco transgenic lines expressing CcASP-RICH were analyzed for Ca²⁺ distribution, ROS, proton gradient, as well as cytoskeleton and cell wall. CcASP-RICH modulated Ca²⁺ content and consequently affected cytoskeleton organization and the deposition of cell wall components. In turn, this affected the growth pattern of pollen tubes. Although the expression of CcASP-RICH did not exert a remarkable effect on the growth rate of pollen tubes, effects at the level of growth pattern suggest that the expression of ASP-RICH may exert a regulatory action on the mechanism of plant cell growth. Full article

(This article belongs to the Special Issue Pollen-Pistil Interaction)

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18 pages, 4836 KiB

Open AccessArticle

Integrated Methylome and Transcriptome Analysis Provides Insights into the DNA Methylation Underlying the Mechanism of Cytoplasmic Male Sterility in Kenaf (Hibiscus cannabinus L.)

by Zengqiang Li, Dengjie Luo, Meiqiong Tang, Shan Cao, Jiao Pan, Wenxian Zhang, Yali Hu, Jiao Yue, Zhen Huang, Ru Li and Peng Chen

Int. J. Mol. Sci. 2022, 23(12), 6864; https://0-doi-org.brum.beds.ac.uk/10.3390/ijms23126864 - 20 Jun 2022

Cited by 5 | Viewed by 1754

Abstract

Cytoplasmic male sterility (CMS) is widely exploited in hybrid seed production. Kenaf is an important fiber crop with high heterosis. The molecular mechanism of kenaf CMS remains unclear, particularly in terms of DNA methylation. Here, using the anthers of a kenaf CMS line (P3A) and its maintainer line (P3B), comparative physiological, DNA methylation, and transcriptome analyses were performed. The results showed that P3A had considerably lower levels of IAA, ABA, photosynthetic products and ATP contents than P3B. DNA methylome analysis revealed 650 differentially methylated genes (DMGs) with 313 up- and 337 down methylated, and transcriptome analysis revealed 1788 differentially expressed genes (DEGs) with 558 up- and 1230 downregulated genes in P3A compared with P3B. Moreover, 45 genes were characterized as both DEGs and DMGs, including AUX,CYP, BGL3B, SUS6, AGL30 and MYB21. Many DEGs may be regulated by related DMGs based on methylome and transcriptome studies. These DEGs were involved in carbon metabolism, plant hormone signal transduction, the TCA cycle and the MAPK signaling pathway and were shown to be important for CMS in kenaf. These results provide new insights into the epigenetic mechanism of CMS in kenaf and other crops. Full article

(This article belongs to the Special Issue Pollen-Pistil Interaction)

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22 pages, 5251 KiB

Open AccessArticle

Rapid Identification of Pollen- and Anther-Specific Genes in Response to High-Temperature Stress Based on Transcriptome Profiling Analysis in Cotton

by Rui Zhang, Lili Zhou, Yanlong Li, Huanhuan Ma, Yawei Li, Yizan Ma, Rongjie Lv, Jing Yang, Weiran Wang, Aierxi Alifu, Xianlong Zhang, Jie Kong and Ling Min

Int. J. Mol. Sci. 2022, 23(6), 3378; https://0-doi-org.brum.beds.ac.uk/10.3390/ijms23063378 - 21 Mar 2022

Cited by 9 | Viewed by 2187

Abstract

Anther indehiscence and pollen sterility caused by high temperature (HT) stress have become a major problem that decreases the yield of cotton. Pollen- and anther-specific genes play a critical role in the process of male reproduction and the response to HT stress. In order to identify pollen-specific genes that respond to HT stress, a comparative transcriptome profiling analysis was performed in the pollen and anthers of Gossypium hirsutum HT-sensitive Line H05 against other tissue types under normal temperature (NT) conditions, and the analysis of a differentially expressed gene was conducted in the pollen of H05 under NT and HT conditions. In total, we identified 1111 pollen-specific genes (PSGs), 1066 anther-specific genes (ASGs), and 833 pollen differentially expressed genes (DEGs). Moreover, we found that the late stage of anther included more anther- and pollen-specific genes (APSGs). Stress-related cis-regulatory elements (CREs) and hormone-responsive CREs are enriched in the promoters of APSGs, suggesting that APSGs may respond to HT stress. However, 833 pollen DEGs had only 10 common genes with 1111 PSGs, indicating that PSGs are mainly involved in the processes of pollen development and do not respond to HT stress. Promoters of these 10 common genes are enriched for stress-related CREs and MeJA-responsive CREs, suggesting that these 10 common genes are involved in the process of pollen development while responding to HT stress. This study provides a pathway for rapidly identifying cotton pollen-specific genes that respond to HT stress. Full article

(This article belongs to the Special Issue Pollen-Pistil Interaction)

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20 pages, 4333 KiB

Open AccessArticle

MAP3Kε1/2 Interact with MOB1A/1B and Play Important Roles in Control of Pollen Germination through Crosstalk with JA Signaling in Arabidopsis

by Juan Mei, Pengmin Zhou, Yuejuan Zeng, Binyang Sun, Liqun Chen, De Ye and Xueqin Zhang

Int. J. Mol. Sci. 2022, 23(5), 2683; https://0-doi-org.brum.beds.ac.uk/10.3390/ijms23052683 - 28 Feb 2022

Cited by 3 | Viewed by 2002

Abstract

Restriction of pollen germination before the pollen grain is pollinated to stigma is essential for successful fertilization in angiosperms. However, the mechanisms underlying the process remain poorly understood. Here, we report functional characterization of the MAPKKK kinases, MAP3Kε1 and MAP3Kε2, involve in control of pollen germination in Arabidopsis. The two genes were expressed in different tissues with higher expression levels in the tricellular pollen grains. The map3kε1 map3kε2 double mutation caused abnormal callose accumulation, increasing level of JA and precocious pollen germination, resulting in significantly reduced seed set. Furthermore, the map3kε1 map3kε2 double mutations obviously upregulated the expression levels of genes in JA biosynthesis and signaling. The MAP3Kε1/2 interacted with MOB1A/1B which shared homology with the core components of Hippo singling pathway in yeast. The Arabidopsis mob1a mob1b mutant also exhibited a similar phenotype of precocious pollen germination to that in map3kε1 map3kε2 mutants. Taken together, these results suggested that the MAP3Kεs interacted with MOB1s and played important role in restriction of the precocious pollen germination, possibly through crosstalk with JA signaling and influencing callose accumulation in Arabidopsis. Full article

(This article belongs to the Special Issue Pollen-Pistil Interaction)

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15 pages, 2093 KiB

Open AccessArticle

A Cysteine-Rich Protein, SpDIR1L, Implicated in S-RNase-Independent Pollen Rejection in the Tomato (Solanum Section Lycopersicon) Clade

by Juan Vicente Muñoz-Sanz, Alejandro Tovar-Méndez, Lu Lu, Ru Dai and Bruce McClure

Int. J. Mol. Sci. 2021, 22(23), 13067; https://0-doi-org.brum.beds.ac.uk/10.3390/ijms222313067 - 02 Dec 2021

Cited by 4 | Viewed by 1847

Abstract

Tomato clade species (Solanum sect. Lycopersicon) display multiple interspecific reproductive barriers (IRBs). Some IRBs conform to the SI x SC rule, which describes unilateral incompatibility (UI) where pollen from SC species is rejected on SI species’ pistils, but reciprocal pollinations are successful. However, SC x SC UI also exists, offering opportunities to identify factors that contribute to S-RNase-independent IRBs. For instance, SC Solanum pennellii LA0716 pistils only permit SC Solanum lycopersicum pollen tubes to penetrate to the top third of the pistil, while S. pennellii pollen penetrates to S. lycopersicum ovaries. We identified candidate S. pennellii LA0716 pistil barrier genes based on expression profiles and published results. CRISPR/Cas9 mutants were created in eight candidate genes, and mutants were assessed for changes in S. lycopersicum pollen tube growth. Mutants in a gene designated Defective in Induced Resistance 1-like (SpDIR1L), which encodes a small cysteine-rich protein, permitted S. lycopersicum pollen tubes to grow to the bottom third of the style. We show that SpDIR1L protein accumulation correlates with IRB strength and that species with weak or no IRBs toward S. lycopersicum pollen share a 150 bp deletion in the upstream region of SpDIR1L. These results suggest that SpDIR1L contributes to an S-RNase-independent IRB. Full article

(This article belongs to the Special Issue Pollen-Pistil Interaction)

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23 pages, 10255 KiB

Open AccessArticle

Identification and Analysis of Genes Involved in Double Fertilization in Rice

by Li You, Li Yu, Ronghong Liang, Ruhao Sun, Fan Hu, Xiaoyun Lu and Jie Zhao

Int. J. Mol. Sci. 2021, 22(23), 12850; https://0-doi-org.brum.beds.ac.uk/10.3390/ijms222312850 - 27 Nov 2021

Cited by 6 | Viewed by 2613

Abstract

Double fertilization is a key determinant of grain yield, and the failure of fertilization during hybridization is one important reason for reproductive isolation. Therefore, fertilization has a very important role in the production of high-yield and well-quality hybrid of rice. Here, we used RNA sequencing technology to study the change of the transcriptome during double fertilization with the help of the mutant fertilization barrier (feb) that failed to finish fertilization process and led to seed abortion. The results showed that 1669 genes were related to the guided growth of pollen tubes, 332 genes were involved in the recognition and fusion of the male–female gametes, and 430 genes were associated with zygote formation and early free endosperm nuclear division. Among them, the genes related to carbohydrate metabolism; signal transduction pathways were enriched in the guided growth of pollen tubes, the genes involved in the photosynthesis; fatty acid synthesis pathways were activated by the recognition and fusion of the male–female gametes; and the cell cycle-related genes might play an essential role in zygote formation and early endosperm nuclear division. Furthermore, among the 1669 pollen tube-related genes, it was found that 7 arabinogalactan proteins (AGPs), 1 cysteine-rich peptide (CRP), and 15 receptor-like kinases (RLKs) were specifically expressed in anther, while 2 AGPs, 7 CRPs, and 5 RLKs in pistil, showing obvious unequal distribution which implied they might play different roles in anther and pistil during fertilization. These studies laid a solid foundation for revealing double fertilization mechanism of rice and for the follow-up investigation. Full article

(This article belongs to the Special Issue Pollen-Pistil Interaction)

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16 pages, 2472 KiB

Open AccessArticle

Pistil Mating Type and Morphology Are Mediated by the Brassinosteroid Inactivating Activity of the S-Locus Gene BAHD in Heterostylous Turnera Species

by Courtney M. Matzke, Hasan J. Hamam, Paige M. Henning, Kyra Dougherty, Joel S. Shore, Michael M. Neff and Andrew G. McCubbin

Int. J. Mol. Sci. 2021, 22(19), 10603; https://0-doi-org.brum.beds.ac.uk/10.3390/ijms221910603 - 30 Sep 2021

Cited by 12 | Viewed by 1950

Abstract

Heterostyly is a breeding system that promotes outbreeding through a combination of morphological and physiological floral traits. In Turnera these traits are governed by a single, hemizygous S-locus containing just three genes. We report that the S-locus gene, BAHD, is mutated and encodes a severely truncated protein in a self-compatible long homostyle species. Further, a self-compatible long homostyle mutant possesses a T. krapovickasii BAHD allele with a point mutation in a highly conserved domain of BAHD acyl transferases. Wild type and mutant TkBAHD alleles were expressed in Arabidopsis to assay for brassinosteroid (BR) inactivating activity. The wild type but not mutant allele caused dwarfism, consistent with the wild type possessing, but the mutant allele having lost, BR inactivating activity. To investigate whether BRs act directly in self-incompatibility, BRs were added to in vitro pollen cultures of the two mating types. A small morph specific stimulatory effect on pollen tube growth was found with 5 µM brassinolide, but no genotype specific inhibition was observed. These results suggest that BAHD acts pleiotropically to mediate pistil length and physiological mating type through BR inactivation, and that in regard to self-incompatibility, BR acts by differentially regulating gene expression in pistils, rather than directly on pollen. Full article

(This article belongs to the Special Issue Pollen-Pistil Interaction)

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21 pages, 4691 KiB

Open AccessArticle

A Rapid Pipeline for Pollen- and Anther-Specific Gene Discovery Based on Transcriptome Profiling Analysis of Maize Tissues

by Yannan Shi, Yao Li, Yongchao Guo, Eli James Borrego, Zhengyi Wei, Hong Ren, Zhengqiang Ma and Yuanxin Yan

Int. J. Mol. Sci. 2021, 22(13), 6877; https://0-doi-org.brum.beds.ac.uk/10.3390/ijms22136877 - 26 Jun 2021

Cited by 6 | Viewed by 2747

Abstract

Recently, crop breeders have widely adopted a new biotechnology-based process, termed Seed Production Technology (SPT), to produce hybrid varieties. The SPT does not produce nuclear male-sterile lines, and instead utilizes transgenic SPT maintainer lines to pollinate male-sterile plants for propagation of nuclear-recessive male-sterile lines. A late-stage pollen-specific promoter is an essential component of the pollen-inactivating cassette used by the SPT maintainers. While a number of plant pollen-specific promoters have been reported so far, their usefulness in SPT has remained limited. To increase the repertoire of pollen-specific promoters for the maize community, we conducted a comprehensive comparative analysis of transcriptome profiles of mature pollen and mature anthers against other tissue types. We found that maize pollen has much less expressed genes (>1 FPKM) than other tissue types, but the pollen grain has a large set of distinct genes, called pollen-specific genes, which are exclusively or much higher (100 folds) expressed in pollen than other tissue types. Utilizing transcript abundance and correlation coefficient analysis, 1215 mature pollen-specific (MPS) genes and 1009 mature anther-specific (MAS) genes were identified in B73 transcriptome. These two gene sets had similar GO term and KEGG pathway enrichment patterns, indicating that their members share similar functions in the maize reproductive process. Of the genes, 623 were shared between the two sets, called mature anther- and pollen-specific (MAPS) genes, which represent the late-stage pollen-specific genes of the maize genome. Functional annotation analysis of MAPS showed that 447 MAPS genes (71.7% of MAPS) belonged to genes encoding pollen allergen protein. Their 2-kb promoters were analyzed for cis-element enrichment and six well-known pollen-specific cis-elements (AGAAA, TCCACCA, TGTGGTT, [TA]AAAG, AAATGA, and TTTCT) were found highly enriched in the promoters of MAPS. Interestingly, JA-responsive cis-element GCC box (GCCGCC) and ABA-responsive cis-element-coupling element1 (ABRE-CE1, CCACC) were also found enriched in the MAPS promoters, indicating that JA and ABA signaling likely regulate pollen-specific MAPS expression. This study describes a robust and straightforward pipeline to discover pollen-specific promotes from publicly available data while providing maize breeders and the maize industry a number of late-stage (mature) pollen-specific promoters for use in SPT for hybrid breeding and seed production. Full article

(This article belongs to the Special Issue Pollen-Pistil Interaction)

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Review

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14 pages, 628 KiB

Open AccessReview

Male Fertility under Environmental Stress: Do Polyamines Act as Pollen Tube Growth Protectants?

by Iris Aloisi, Chiara Piccini, Giampiero Cai and Stefano Del Duca

Int. J. Mol. Sci. 2022, 23(3), 1874; https://0-doi-org.brum.beds.ac.uk/10.3390/ijms23031874 - 07 Feb 2022

Cited by 7 | Viewed by 2114

Abstract

Although pollen structure and morphology evolved toward the optimization of stability and fertilization efficiency, its performance is affected by harsh environmental conditions, e.g., heat, cold, drought, pollutants, and other stressors. These phenomena are expected to increase in the coming years in relation to predicted environmental scenarios, contributing to a rapid increase in the interest of the scientific community in understanding the molecular and physiological responses implemented by male gametophyte to accomplish reproduction. Here, after a brief introduction summarizing the main events underlying pollen physiology with a focus on polyamine involvement in its development and germination, we review the main effects that environmental stresses can cause on pollen. We report the most relevant evidence in the literature underlying morphological, cytoskeletal, metabolic and signaling alterations involved in stress perception and response, focusing on the final stage of pollen life, i.e., from when it hydrates, to pollen tube growth and sperm cell transport, with these being the most sensitive to environmental changes. Finally, we hypothesize the molecular mechanisms through which polyamines, well-known molecules involved in plant development, stress response and adaptation, can exert a protective action against environmental stresses in pollen by decoding the essential steps and the intersection between polyamines and pollen tube growth mechanisms. Full article

(This article belongs to the Special Issue Pollen-Pistil Interaction)

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9 pages, 546 KiB

Open AccessReview

Challenges and Perspectives in the Study of Self-Incompatibility in Orchids

by Xiaojing Zhang, Yin Jia, Yang Liu, Duanfen Chen, Yibo Luo and Shance Niu

Int. J. Mol. Sci. 2021, 22(23), 12901; https://0-doi-org.brum.beds.ac.uk/10.3390/ijms222312901 - 29 Nov 2021

Cited by 5 | Viewed by 2931

Abstract

Self-incompatibility affects not only the formation of seeds, but also the evolution of species diversity. A robust understanding of the molecular mechanisms of self-incompatibility is essential for breeding efforts, as well as conservation biology research. In recent years, phenotypic and multiple omics studies have revealed that self-incompatibility in Orchidaceae is mainly concentrated in the subfamily Epidendroideae, and the self-incompatibility phenotypes are diverse, even in the same genus, and hormones (auxin and ethylene), and new male and female determinants might be involved in SI response. This work provides a good foundation for future studies of the evolution and molecular mechanisms of self-incompatibility. We review recent research progress on self-incompatibility in orchids at the morphological, physiological, and molecular levels, provide a general overview of self-incompatibility in orchids, and propose future research directions. Full article

(This article belongs to the Special Issue Pollen-Pistil Interaction)

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17 pages, 1784 KiB

Open AccessReview

Signaling at Physical Barriers during Pollen–Pistil Interactions

by Kayleigh J. Robichaux and Ian S. Wallace

Int. J. Mol. Sci. 2021, 22(22), 12230; https://0-doi-org.brum.beds.ac.uk/10.3390/ijms222212230 - 12 Nov 2021

Cited by 8 | Viewed by 3071

Abstract

In angiosperms, double fertilization requires pollen tubes to transport non-motile sperm to distant egg cells housed in a specialized female structure known as the pistil, mediating the ultimate fusion between male and female gametes. During this journey, the pollen tube encounters numerous physical barriers that must be mechanically circumvented, including the penetration of the stigmatic papillae, style, transmitting tract, and synergid cells as well as the ultimate fusion of sperm cells to the egg or central cell. Additionally, the pollen tube must maintain structural integrity in these compact environments, while responding to positional guidance cues that lead the pollen tube to its destination. Here, we discuss the nature of these physical barriers as well as efforts to genetically and cellularly identify the factors that allow pollen tubes to successfully, specifically, and quickly circumnavigate them. Full article

(This article belongs to the Special Issue Pollen-Pistil Interaction)

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