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. 2024 Feb 24;75(14):4210–4218. doi: 10.1093/jxb/erae071

The maternal embrace: the protection of plant embryos

Sjoerd Woudenberg 1, Feras Hadid 2, Dolf Weijers 3,✉, Cecilia Borassi 4
Editor: Pablo Manavella5
PMCID: PMC11263485  PMID: 38400751

Abstract

All land plants—the embryophytes—produce multicellular embryos, as do other multicellular organisms, such as brown algae and animals. A unique characteristic of plant embryos is their immobile and confined nature. Their embedding in maternal tissues may offer protection from the environment, but also physically constrains development. Across the different land plants, a huge discrepancy is present between their reproductive structures whilst leading to similarly complex embryos. Therefore, we review the roles that maternal tissues play in the control of embryogenesis across land plants. These nurturing, constraining, and protective roles include both direct and indirect effects. In this review, we explore how the maternal surroundings affect embryogenesis and which chemical and mechanical barriers are in place. We regard these questions through the lens of evolution, and identify key questions for future research.

Keywords: Archegonia, embryo development, embryogenesis, land plants, maternal tissue, mechanical barrier

Maternal tissues play a role in nurturing, protecting, and constraining the plant embryo. In this review, we discuss the effects these roles have in controlling embryogenesis across land plants.

Introduction

Transition from an aquatic environment to land required the development of specialized structures that allowed plants to survive and reproduce. These innovations included adaptations to abiotic stresses such as drought, exposure to UV-B light, and temperature change. In this context, adaptation to land involved the zygote developing into a multicellular diploid organism, the embryo, in contrast to what we see in the green algal sister groups (Graham et al., 1991; Domozych and Bagdan, 2022; von der Heyde and Hallmann, 2022). The embryo develops into the sporophyte, embedded in and surrounded by maternal tissue, which marks a key innovation during land plant evolution. In bryophytes and ferns, the egg cell and embryo are enclosed by only a single cell layer of the archegonium. During fertilization, the archegonium is open to enable entry of motile sperm, resulting in a high vulnerability to biotic and abiotic stressors. In flowering plants, the embryo is isolated from the environment, located inside the embryo sac; surrounded by the endosperm and integuments. Vascular plants (which develop a complex sporophyte) either do (ferns) or do not (flowering plants) have archegonia. This suggests that an increase in the maternal tissues surrounding the embryo was not crucial to establish complexity. The maternal surroundings can offer protection from the environment but can also constrain and direct embryo development. Here we give an overview of the reproductive structures in land plants and the differences among them. By comparing these reproductive structures across land plants and their effects on development, mechanics, and molecular regulation, we try to shed light on the roles that maternal tissues play in controlling embryogenesis.

The role of maternal tissues during plant embryo development

The embryo, as a product of fertilization, is genetically distinct from the surrounding tissue and has a different ploidy. It can therefore, in this context, be regarded as a different generation and even a distinct organism. Other reviews discuss plant embryogenesis in flowering plants in detail (e.g. Bayer et al., 2017; Radoeva et al., 2019; Rensing and Weijers, 2021; Reyes-Olalde et al., 2023). However, one element that is missing from most recent perspectives is the widely different morphologies and life histories among the entire group of embryo-bearing plants. Nevertheless, it should be noted that beyond anything else, the type and amount of maternal tissue are highly divergent between the different plant taxa (Box 1). In short, it ranges from a single cell layer in bryophytes, lycophytes, and ferns, to complex multi-layered seed and fruit tissues in seed plants and flowering plants. The evolution of dominant sporophytes is correlated with an increase of maternal protective structures. In the end, both archegonia and seeds can sustain complex embryo formation including 3D axis establishment while providing different degrees of confinement and protection. This is clearly observed when comparing embryos in archegonia of the fern Ceratopteris richardii (Aragón-Raygoza et al., 2020; Conway and Di Stilio, 2020) with Arabidopsis thaliana embryos inside seeds (Yoshida et al., 2014).

Box 1. Diversity in reproductive structures among embryophytes.

In all non-flowering plants, the egg cell and later the embryo are immersed in the archegonium. The archegonium is a single cell layer surrounding the egg cell on all sides except the top, leaving a neck-like structure that facilitates sperm entry upon fertilization. The largest phenotypic differences exist in hornworts and leptosporangiate ferns where archegonia are sunken into the tissue (±3 cells) and the neck barely sticks out (Frangedakis et al., 2021). This neck is closed prior to fertilization, but increased maturation of the egg cell leads to degradation of the canal cells allowing sperm entry due to chemotaxis. In seed plants, the egg cell is contained by multiple tissue layers. Inside the ovule, the egg cell is surrounded by the nucellus and by one or two integuments in gymnosperms and angiosperms, respectively. In angiosperms, double fertilization gives rise to the endosperm, a tissue that surrounds the embryo and is absorbed by it (as in A. thaliana) or remains present in the mature seed (as in Z. mays). Both the embryo and the endosperm develop enclosed by the maternal tissue that later forms the seed coat (Baroux et al., 2002). In gymnosperms, archegonia are still present inside the integuments (each one carrying one egg cell), making them an evolutionarily intermediate structure.

Box 1. Diversity in reproductive structures among embryophytes

Also, the maternal tissue in seed plants is connected to the embryo by the suspensor which has a crucial role in embryogenesis by providing signalling input and nutrients to the embryo (Yeung and Meinke, 1993; Robert and Friml, 2009). Importantly, the embryo itself also plays a role in controlling these exchanges. In Arabidopsis, the embryo is involved in the production of three extra-embryonic barriers: the envelope (Harnvanichvech et al., 2023), the cuticle (Fourquin et al., 2016; Creff et al., 2019), and the sheath (Doll et al., 2020) (Fig. 1). The protective role of the cuticle and the sheath is well established, while the recently discovered envelope might be acting as a diffusion barrier or mechanical constraint to the embryo very early during development when the constraint established by the endosperm and seed coat is absent.

Fig. 1.

Fig. 1.

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Schematic representation of the development of non-seed and seed plant embryos, and the chronical order in which protective structures are formed or grow around the Arabidopsis embryo. The bottom panel depicts all the stressors by which plant embryos can be influenced, ranging from abiotic to biotic agents; note that in both cases pathways convey to chemical and mechanical effectors and that hormones are not explicitly mentioned but are an integral part of chemical signalling.

Taken together, the embryo is influenced by the surrounding maternal tissue and there is a flow of nutrients and hormones between them. However, given that the embryo is physically surrounded by maternal tissues, it is not easy to derive whether the role of these maternal tissues in protecting or constraining the embryo is active or passive. Does the maternal tissue protect the embryo from abiotic and biotic stresses? Does it provide a mechanical context that is conducive to embryo development? (Fig. 1). In this review, we explore how maternal tissues are or might be involved in embryo development across land plants.

The maternal tissue as a diffusion barrier

It is well known that the maternal tissue provides an important chemical barrier, or at least a separation, since there is an active control of which molecules can enter. For example, glucosinilates, a class of defensive compounds, are produced in the funiculus and then transported into the maturing seed in Arabidopsis (Xu et al., 2023). Similarly, auxin is transported from the maternal integuments, through the suspensor into the embryo by PIN proteins, where it helps control development (Friml et al., 2003; Grieneisen et al., 2007; Robert et al., 2013, 2018; Wabnik et al., 2013). It has also been shown that brassinosteroids are involved in signalling between the maternal seed coat and the endosperm (Lima et al., 2023, Preprint). These hormonal exchanges seem very conserved in most angiosperms (Florez-Rueda et al., 2023, Preprint). Likewise, the central cell-derived ESF1 peptides contribute to proper embryo development (Costa et al., 2014), and even maternal morphogenetic signals are suggested to be involved in embryo patterning in Arabidopsis (Ray et al., 1996). In addition to an active mode of transport, many molecules depend on a more passive mode of transport. Oxygen, required for active respiration necessary for fast growth, depends only on diffusion and convection as far as currently understood (Loreti and Perata, 2020). Given that oxygen can act as a developmental, diffusible signal in the shoot (Weits et al., 2021), it is possible that the array of diffusion barriers that separate the embryo from the atmosphere regulate development through controlling oxygen availability. The embryo is often only locally symplastically connected to the mother via a placenta/suspensor. Therefore, no apoplastic diffusion can take place over most of the embryo surface, limiting passive transport considerably.

Controlled, active transport of molecules is much less constrained by the presence of maternal tissue as there are often specialized transporters present aiding in making specific gradients. For example, auxin-induced transcription seems concentrated around the maize megaspore mother cell and in developing female gametophytes in Arabidopsis (Lituiev et al., 2013), which resembles the pattern observed in the archegonia of bryophytes (Fujita et al., 2008; Landberg et al., 2013, 2021). A recent model has been proposed for lateral root initiation, where the difference between turgor pressure and cell wall pressure controls auxin fluxes (Ramos et al., 2023, Preprint). The modelling directly links auxin gradients to tissue stress. This can lead to the inference that maternal tissues could potentially impose tissue stresses on the embryo and thus influence auxin patterns.

The maternal tissue as a mechanical constraint

In animals, there is evidence that mechanical cues are responsible for cell fate determination and organ size during embryogenesis, as was observed in mouse blastocysts where lumenal pressure affects cell fate determination and embryo size (Day and Lawrence, 2000; Navis and Nelson, 2016; Chan et al., 2019). Similarly, the mechanical interplay between the endosperm and the maternally derived seed coat plays a role in embryo development and in seed size and shape. It has been shown that genetic ablation of the Arabidopsis endosperm inhibits seed growth and causes defects in embryo growth and cell division (Weijers et al., 2003), suggesting that proper endosperm development plays a role during early embryo development. In addition, it was shown that the tension created by the endosperm on the outer integument is responsible for directing seed growth (Bauer et al., 2023), and such drastic changes in endosperm turgor pressure are registered while the embryo transitions from the pre-globular to the heart stage (Creff et al., 2023), indicating that cell differentiation and patterning processes are occurring at the same time as these changes in tension during seed growth take place. All these point to the importance of the mechanical balance inside the seed provided by the constraints imposed by the maternal tissues and the endosperm on the developing embryo inside the seed.

Limited information is available for archegonium-encapsulated embryos. However, some examples are present for mosses and ferns. Experimentally removing the calyptra (archegonial remnants) around the young sporophyte from the moss Funaria inhibits differentiation and leads to abnormal growth, with an increase in lateral cell numbers, and alters division planes (French and Paolillo, 1975, 1976). Similarly, in ferns when the calyptra is removed, there is a reduction of differentiation leading to a cellular gametophytic mass at early stages and adventitious-like shoot formation later (Ward and Wetmore, 1954; Demaggio and Wetmore, 1961). Finally, in hornwort and fern embryos, within more embedded archegonia, the first division is parallel to the longitudinal axis of the archegonium (Renzaglia, 1978; Frangedakis et al., 2021), in contrast to the more naked archegonia in the other bryophytes. This suggests a role for the maternal tissue in embryo development by shaping and controlling cell division orientation and proliferation, possibly due to steering tissue stress mechanics or hormonal control.

Evolutionary trade-offs

It is clear that there are large structural differences between the maternal structures surrounding embryos in land plants, which are correlated with different degrees of constraint and protection during embryogenesis. However, evolutionary forces are often hard to predict due to multitrophic effects, and it is not easy to infer what might have been the drivers for the various morphologies. Prior to the process of embryogenesis, an important step needs to take place: fertilization. In all plant reproductive structures, the fertilization site is fixed, but the modes and mechanisms of fertilization are completely different between species. In bryophytes and ferns, fertilization is dependent upon motile sperm entering the archegonium, while flowering plants depend on invasive pollen tube growth from the stigma, through the transmitting tract towards the ovules.

Egg cells located in archegonia are much more accessible to the environment; they are literally in direct contact with it. However, accessibility to a motile sperm (±4 µm width) (Renzaglia et al., 2002) might also open the door to bacteria and fungi, and would also expose the egg cell and embryo to the abiotic environment. We explored whether publicly available expression data show signatures of stress response or immune response in embryos. Interestingly, there appears to be an enrichment of genes related to oxidative stress in the Marchantia egg cell (Kawamura et al., 2022). In contrast, the many barriers and enclosing tissues in flowering plants would limit the ability for pathogens to invade the egg cell. We also explored public transcriptome resources to ask if there are signs of response to environmental stress signals or pathogens in Arabidopsis embryos. Early embryo transcriptomes appear enriched in genes involved in biotic stress. Among these are abscisic acid (ABA)-responsive genes (ERF15 and PR14/LTP3) and to a lesser extent jasmonic acid (JA)- and salicylic acid (SA)-responsive genes (Hofmann et al., 2019). However, the most studied stress-induced genes (e.g. PR1 and ERF1) are not expressed or tend to only increase their expression levels after early embryogenesis (e.g. MYC2, EIN3, and BAK1) (Hofmann et al., 2019). Maize and rice only show biotic stress signatures during later stages of embryogenesis (Xu et al., 2012; Chen et al., 2014; Zhang et al., 2023). This suggests that, even in the deeply embedded Arabidopsis embryo, there may be an active response to biotic stress. Given that these patterns of expression were inferred from experiments that were not intended to test stress response in embryos—and lacked controls to rigorously test this—an important question is to what degree embryogenesis across land plants is accompanied by active responses to environmentally induced stresses.

One difficulty in comparing and understanding the different mechanisms and roles of the reproductive tissues is the large evolutionary gap between them. Ideally, closely related sister species, with highly dissimilar reproductive structures, from different environments would be compared. In that way, the adaptive value of a certain trait (e.g. thicker integuments) could be inferred. Different Arabidopsis ecotypes have been assayed for variation in, for example, megaspore formation, flower morphology, and timing (Rodríguez-Leal et al., 2015; Sellami et al., 2019; Kinmonth-Schultz et al., 2021; Yan et al., 2021), but reproductive structures are probably too similar in this species to identify meaningful correlations with stress sensitivity for reproductive success.

Arabidopsis as a mechanistic model

Rather than natural variants, Arabidopsis mutants lacking (or having reduced) layers of maternal tissue provide an excellent resource to functionally understand the role of maternal tissue in embryogenesis. Mutant phenotypes differ drastically between having no endosperm to lacking one of the two integuments (see Table 1). In very severe mutants, lethality and abortion are very common, which is the case for many of the listed mutants. However, less severe mutants show clear defects in embryo growth and patterning. Many of these mutants have not been explicitly assayed for effects on embryo patterning, or to determine if embryogenesis is more sensitive to the environment. Moreover, not all the integument/endosperm mutants in Arabidopsis are arrested at the same stage. There are complex sets of genes and signalling pathways that regulate their growth and development, and the interplay and crosstalk between the embryo and the maternal tissue is not fully understood. Although for many of these genes, no information is available on the role of orthologues in other species, there are morphologically similar mutants. In barley, recessive maternal effect mutants were described to have a shrunken endosperm phenotype (Felker et al., 1985). Similarly, it was found that FBP7 and FBP11 MADS-box genes in petunia have a role in seed development by controlling endosperm and seed coat development (Colombo et al., 1997). Thus, across multiple flowering plant species, these maternal tissues play an important, but poorly understood, role in embryo development.

Table 1.

Overview of maternal defect mutants in Arabidopsis and their phenotypic arrests

Phenotypic group Mutant Protein function Description Reference
Defects in endosperm development haiku1 (iku1) VQ-motif-containing proteinVQ-motif-containing protein

  • Precocious cellularization.

  • Reduced embryo size.

  • Reduced proliferation after the torpedo stage.

  • Unaffected early morphogenesis.

  • 10% lethal embryos at the globular stage when endosperms cellularize at stage Vll.

  • Integuments elongate less.

 Garcia et al. (2003)
haiku2 (iku2)
endosperm defective1 (ede1-1) Microtubule-binding protein

  • Absence of cellularization.

 Pignocchi et al. (2009)

  • Aberrant microtubule cytoskeleton.

  • 40% of the embryos are arrested after the globular stage.

  • 26% abort earlier than the globular stage.

  • Full knockout is lethal.

  • Cell division defects at globular and heart stages.
B sister gemes (tt16/abs), shatterproof 1 and 2 (shp1 and shp2) Agamous-like MADS-box protein

  • Defects in the cell divisions during ovule and seed coat development.

 Ehlers et al. (2016)

  • Malformed seedlings, fused organs, not uniform.

  • Mechanically constrained embryos.

  • Triple mutant shows 33% lethality, other 20% malformed

  • Smaller cavity, squeezed aborted embryos.
capulet (cap) /

  • cap1 early arrest between zygote and two-cell stage.

 Grini et al. (2002)

  • cap2 is not arrested as early as cap1 and could develop till the early heart stage.

  • cap1 endosperm stops dividing shortly after the initial early syncytial mitotic divisions.
Defects in integument development short integuments 1 and 2 SIN1: Dicer homologue

  • Ovules with shorter or absent integuments.

  • Reduction in cell number and abnormal growth of the integuments.

 Broadhvest et al. (2000)
(sin1 and sin2) SIN2: GTPase

  • Full knockout is lethal.
superman (sup) Transcriptional regulator

  • Symmetric growth of the outer integument.

 Gaiser et al. (1995)

  • Ovules are elongated and tubular at anthesis.

  • Reduced seed number (partial infertility at middle to late stage).
inner no outer (ino) INO: YABBY

  • Absence of outer integument growth on both sides of the ovule primordium.

 Villanueva et al. (1999)

  • Reduced dormancy in single mutant.
aintegumenta (ant) ANT: AP2-like transcription factor

  • Double mutant (ino/ant) has no embryo sac formation.

 Baker et al. (1997); Schneitz et al. (1997)

  • Defect at meiosis.
knat3 and knat4 Homeobox protein

  • Inner and outer integument arrested stage 3-II of ovule development.

 Chen et al. (2023)

  • Double mutants have shorter siliques than the wild type, and are not fertile.
megaintegumenta (mnt) Auxin response factor

  • Increased seed size and weight.

 Schruff et al. (2006)

  • Enlarged seed coats.

  • Slower embryo development.

  • Bigger embryos.

  • Increased divisions of integuments
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In vitro embryogenesis provides another interesting approach to studying maternal effects on embryogenesis since the maternal tissue is absent in these in vitro embryos (Mordhorst et al., 1997). This aspect is the most obvious in microspore-derived embryos in Brassica napus, a close sister species of Arabidopsis. These microspore-derived embryos only start zygotic-like embryogenesis upon abiotic stress treatments such as heat or cold (Testillano, 2019). However, early patterning is less ordered than during zygotic embryogenesis, organs are formed later and are sometimes anatomically different, and embryo maturation (i.e. desiccation) is absent (Mordhorst et al., 1997; Ilić-Grubor et al., 1998; Seguí-Simarro et al., 2008; Soriano et al., 2013, 2014). Some culture methods allow for the formation of zygotic-like in vitro embryos that closely match zygotic division patterns (Supena et al., 2008; Corral-Martínez et al., 2020). Most culture methods use high concentrations of sucrose or polyethylene glycol (PEG), leading to a high osmolarity which might mimic the mechanical properties of the ovule on the embryo. The initial stress-induced reprogramming of the microspore and the later necessity for high osmolality clearly shows the role of stress, and in particular mechanical stress, on embryo development.

Investigating the correlation between maternal tissue phenotypes in these mutants and (in vitro) embryogenesis will help define the functional relationship between these entities. Likewise, it is crucial to understand what molecular pathways underlie the diverse phenotypes of both the explored and unexplored maternal tissue-related mutants. Additionally, it is important to understand how those molecular and signalling pathways intersect with environmental cues in the control of embryogenesis.

Conclusions

In this review, we explore the role of the maternal tissue in embryogenesis, with a focus on how it might protect but also guide the embryo in development (Fig. 1). Many questions remain unanswered (Box 2), as within the field there has been relatively little focus on these aspects. However, there are great resources to start studying these questions in much more detail, as we tried to make clear: from comparing different accessions, different mutants, and even different species. Are these plants more susceptible to environmental perturbations due to lacking or altered maternal tissue? This is a key question, not only for fundamental science, but also in understanding how environmental fluctuations (and climate change) affect seed production and to understand which structures play a pivotal role in that process.

Box 2. Open questions.

  • - Is the embryo buffered from the environment?

  • - How does encapsulation of the embryo in maternal tissues in land plants affect and protect embryo development?

  • - What is the role of extra-embryonic tissues in embryogenesis? How is the increase in complexity of the tissues surrounding the embryo related to this process? Are these tissues constraining and directing embryo development or acting as a protective barrier?

  • - What are the chemical and mechanical constraints imposed by the different reproductive structures/maternal tissues in each taxa? What is the relationship between such differences and the evolution of embryogenesis?

  • - Is the increase in maternal/extra-embryonic tissues surrounding the egg cell (and embryo) required for the increase in body plan complexity in the sporophyte?

Acknowledgements

We would like to thank Dr Joao Ramalho for insightful comments while developing the topic for this review.

Contributor Information

Sjoerd Woudenberg, Laboratory of Biochemistry, Wageningen University, Stippeneng 4, 6708WE Wageningen, The Netherlands.

Feras Hadid, Laboratory of Biochemistry, Wageningen University, Stippeneng 4, 6708WE Wageningen, The Netherlands.

Dolf Weijers, Laboratory of Biochemistry, Wageningen University, Stippeneng 4, 6708WE Wageningen, The Netherlands.

Cecilia Borassi, Laboratory of Biochemistry, Wageningen University, Stippeneng 4, 6708WE Wageningen, The Netherlands.

Pablo Manavella, Instituto de Agrobiotecnología del Litoral, Argentina.

Author contributions

SW, FH, DW, and CB: conceptualization and writing; SW and DW: funding acquisition; DW and CB: supervision.

Conflict of interest

The authors have no competing interests.

Funding

Work related to this review is supported by a grant from the Graduate School Experimental Plant Sciences to SW, and by grants from the European Research Council (ERC; AdG DIRNDL; contract number 833867) and the Netherlands Organization for Scientific Research (NWO; ENW-KLEIN2; OCENW.KLEIN.516) to DW.

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