Expression of some upregulated cell wall‐modifying genes in
Abstract
Seed germination is a complex process in which the embryo, enclosed within the surrounding tissues, must quickly switch from a maturation program to a germination‐driven developmental process that will prepare the embryo for seedling growth and establishment. The germination process initiates with water uptake by the dry seed and culminates, usually, with the radicle protrusion. The radicle emergence from the seed is a highly regulated process that involves discrete and coordinated changes in plant cell wall extensibility and rearrangements of its components, among other processes. In this chapter we will review current knowledge of the physiological process of controlled cell separation and expansion, which give the primary cell wall its plastic properties by “loosening” of the main components of the cell wall during seed germination. We will focus on the physiological importance of primary cell wall constitution and modification by the activity in muro of a broad variety of cell wall‐modifying enzymes that include hydrolases and transglycosylases, as well as non‐enzymatic processes such as expansin‐mediated loosening during seed germination.
Keywords
- cell wall modification
- primary cell wall
- seed germination
1. Introduction
Seeds constitute a critical stage in the life cycle of embryophytes. In this stage, the plant embryo remains in a quiescent state until the proper conditions of temperature, water availability, and, in some species, light are met in order for the processes of germination and seedling establishment to occur [1, 2]. The mature seed contains the embryo, which is surrounded by the seed coat (testa) that is derived from the maternal tissues and in some species by one or more layers of storage tissue (endosperm) [2]. Seeds can function as resistance structures. Several mechanisms have evolved, in tight relation with the environment, to ensure the survival of the quiescent embryo [3]. Part of these mechanisms includes the modification of the structure and composition of plant cell walls.
One characteristic feature of plant cells is that they are enclosed in a polysaccharide and protein matrix, denominated as cell wall [4]. Plant cells can have two different types of wall. Primary walls, produced during cytokinesis, are flexible structures that regulate cell growth and shape. The secondary walls are deposited after the cell has achieved its final size and shape, by the inclusion of lignin and other phenolic compounds, thus making the cell wall rigid and usually impermeable. Cell walls have several functions that include the regulation of cell‐cell adhesion and abscission, apoplastic transport, mechanical support and maintenance of turgor pressure, and defense against pathogens [2, 5]. In seeds, cell walls are modified in order to generate hard, and in some cases impermeable, coats that protect the embryo from the environmental conditions. Also, seed cell walls can store energy that can be mobilized to feed embryo growth and development. Finally, cell walls regulate the timing of seed germination by fine‐tuning the processes of matrix polysaccharide loosening/breakage, as well as the integration of environmental cues with the hormonal and physiological status of the embryo [4, 6]. In this chapter we will focus only on primary cell walls and their importance on seed germination.
2. Seed germination
Seed germination is a physiological process initiated with water uptake and culminating with the emergence of the embryo through its protective tissues, which might include the testa, endosperm, perisperm, or pericarp [2]. The testa and the endosperm rupture must be coordinated with environmental seasonality to facilitate germination in the most favorable conditions [1, 6]. Several mechanisms have evolved to ensure proper synchronization of germination with environmental cues; among these is the interplay of hormonal signaling pathways via abscisic acid (ABA), gibberellins (GA), ethylene, and jasmonates [7–10]. These hormones exert their regulation on germination through different pathways including cell wall remodeling [7, 11].
In the classical model of seed germination described by Bewley et al. [12], the process of germination is divided into three phases, distinguished by the rate of water absorption by the seed tissues. The phase I, or imbibition phase, is characterized by a rapid water uptake rate driven by the difference in water potential between the seed and the environment. In this phase also the reactivation of primary metabolism and DNA repair pathways starts. Next, in phase II or activation phase, the imbibition rate decreases, water content remains stable, and major changes in the metabolic pathways and activation of other cellular processes take place. In this phase the integration of environmental cues with the internal status of the seed that will determine whether or not the seed will enter into the next phase occurs. Finally, in phase III there is another rapid water uptake driven by radicle protrusion and is mainly related to seedling growth. Germination is completed once the radicle has emerged at the onset of phase III. This triphasic model of imbibition can be applied to all seeds analyzed thus far [12, 13]. The imbibition time needed for completion of germination is highly variable among species and even within seed lots, and it depends on several factors like seed history and environmental conditions experienced by the mother plant at the moment of seed dispersion and during the after‐ripening period [12, 14, 15].
It is now generally accepted that radicle protrusion occurs by two nonexclusive processes [2, 13]. The first process involves a decrease in the mechanical resistance of the enclosing tissues, especially in the micropylar region of the testa and endosperm [2, 10]. The second process deals with an increasing growth potential of the embryo, driven by turgor pressure and cellular expansion in the embryonic axis [2, 13]. Most of the knowledge generated about the regulation of radicle protrusion comes from endospermic seeds, where testa and endosperm rupture can occur in two easily distinguishable stages (
In recent years, with the advent of whole genome/transcriptome analysis, it has been possible to study the process of germination with high spatial‐temporal resolution. Transcriptomic analysis allows a comprehensive view of seed germination by dissecting “early” or “late” germination processes, the first being the initial response to water and the second corresponding to the interval from the imbibed seed to the radicle protrusion [14, 15]. Also, in endospermic seeds, an important landmark is the distinction between the processes that occur prior to testa rupture and after it that leads to endosperm rupture [8, 16–18].
Several studies demonstrate that the main transcripts, enzymes, and other proteins accumulated in dry seeds participate in primary metabolism, starch and storage protein mobilization, reactive oxygen species (ROS) scavenging, and cell wall synthesis [14, 15]. Aside from providing building blocks to sustain protein production and cell growth, the reactivation of primary metabolism in the early stages of seed germination plays a major role in the generation of the proper redox state to promote the activity of different enzymes and produce energy to support processes essential for radicle protrusion [14, 19].
In
Gibberellins play a major role in promoting a myriad of developmental programs, and its antagonistic role in ABA‐mediated block of germination has been described [24]. GA stimulates seed germination by enhancing embryo growth; embryos of
An overrepresentation analysis (ORA) of gene ontologies showed that transcription regulation is enriched in both the endosperm and the embryo transcriptomes of
3. Cell wall structure and composition
Plant cell walls are complex and highly dynamic structures composed of a variety of polysaccharides, proteins, and aliphatic or aromatic compounds [28, 29]. They are continually being modified throughout development and in response to environmental stimuli [30, 31]. Primary cell walls of flowering plants can be classified in two main groups depending on its general architecture and composition, as well as their biosynthetic processes [32, 33]. Type I cell walls are the most common, present in dicotyledonous and the non‐commelinoid monocotyledonous plants (a more basal group of aroids, alismatids, and lilioids). Type II cell walls are found only in the commelinoid monocots that include the Poales (members of the families Poaceae, Bromeliaceae, and Cyperaceae) [32, 33].
3.1. Primary cell wall polysaccharides
Primary cell wall polysaccharides constitute the majority of the wall dry mass in land plants and can be grouped in three main classes: cellulose, hemicelluloses, and pectins [30]. Cellulose is a linear 1,4‐β‐d‐glucan that assembles into partially crystalline microfibrils, each of which contains about 36 parallel polysaccharide chains [34]. Cellulose is synthesized
Hemicelluloses are polymers whose backbones consist of β‐glucose, β‐xylose, or β‐mannose, with short side chains. In all vascular plants with type I walls, the most common hemicelluloses are xyloglucans (XyG), whereas type II cell walls contain less XyG, being the most abundant glucuronoarabinoxylans (GAX) and β1,3:β1,4 mixed glucans [33]. Hemicellulose chains adhere to cellulose microfibrils, in a rope‐like manner, to restrain cell expansion [30, 34]. Also, in type I cell walls, hemicelluloses bind and cross‐link with pectin and form the hydrated matrix [30].
The group generally known as pectins comprises over 30% of the cell wall total mass in dicots [31, 36]. Pectins are acidic heteropolymers that form a hydrated gel, in which cellulose and other molecules are embedded in the plant cell wall. Their main defining feature is 1,4‐linked α‐d‐galacturonic acid residues (GalA). Pectins interact covalently and non‐covalently with other pectin molecules or with hemicellulose xyloglucan or arabinogalactans [31]. Several studies support the hypothesis that the three major pectin classes, homoglacturonan (HG), rhamnogalacturonan I, and rhamnogalacturonan II, are covalently linked in the cell wall [29, 37], forming a hydrophilic macromolecular network. Pectin is deposited on the cell wall matrix in a highly methylesterified form [28]. The methyl group is removed by pectin methylesterases (PMEs) in muro, providing an anionically charged matrix and changing the mechanic properties of the cell wall. Increasing evidence shows that the regulation of the degree of methylesterification of the pectic matrix plays a fundamental role in plant growth, development, morphogenesis, cell‐cell adhesion, cell expansion, seed hydration, and seed germination [5, 16, 36, 38].
Other polysaccharides present in primary cell walls of various species are the mannans, arabinoxylans, and arabinogalactans. Mannans are formed by mannosyl residues linked by β‐1,4‐glycosidic linkages. This mannosyl backbone can contain glucose residues (glucomannans) or be further substituted by single galactose residues with α‐1,6‐linkages (galactomannans). Arabinoxylan consists of a (1,4)‐linked β‐d‐xylan backbone decorated with arabinose branches. Other residues, such as glucuronic acid and ferulic acid esters (FAE), are also attached in arabinoxylans that are particularly abundant in cereal grasses. Arabinogalactan and storage xyloglucans are used as reserves in cotyledons. The basic structure of storage xyloglucans differs from the primary wall xyloglucans in that it is not fucosylated [39].
3.2. Cell wall proteins
Primary cell walls are mainly constituted by polysaccharides; however, proteins account for about 10% of the total dry mass of the wall [40]. Proteins that contain a secretion signal peptide, which targets them to the secretory pathway and in most cases is excised to allow activation or proper protein function, are commonly referred as classical cell wall proteins [40–42]. In
3.2.1. Structural proteins
Structural proteins are usually classified by the predominant amino acids in their sequence, although some of them can belong to more than one category. The most common include the hydroxyproline‐rich glycoproteins (HRGPs), the glycine‐rich proteins (GRPs), the proline‐rich proteins (PRPs), and the arabinogalactan proteins (AGPs). These proteins vary greatly in abundance within plant species, cell tissues, and environmental conditions [4]. Arabinogalactan proteins, that are widely distributed among plant families and comprise about 2–10% of the total protein in the wall, are highly glycosylated. Also, AGPs are rich in hydroxyproline, serine, alanine, threonine, and glycine, and resistant to proteolysis in their native state [41]. Extensins are a family of HRGPs particularly abundant in dicots that have been involved in modification of wall extensibility in elongating tissues [43].
3.2.2. Proteins acting on polysaccharides
Within the CWPs acting on polysaccharides, there are a broad variety of activities. For instance, the group of glycosyl hydrolases (GHs) include glycosidases (β‐glucosidase, β‐galactosidase, β‐xylosidase, and α‐xylosidase, and exo‐polygalacturonases) and glycanases like β‐mannanase, β‐xylanase, (1→4)‐β‐glucanase “cellulase”, endo‐polygalacturonases, and xyloglucan endo‐hydrolase (XEH). The combined activity of these kinds of enzymes is theoretically capable of hydrolyzing most of the glycosidic bonds in the cell wall polysaccharides but do not imply that all enzymes are active at the same time or tissue. The glycosyltransferases (GTs) activity involves the formation of a glycosyl‐enzyme complex that is attacked by an acceptor substrate (another oligo/polysaccharide). This activity allows the integration of recently secreted polysaccharides into the matrix and the grafting of polysaccharides already present in the wall matrix [44]. This category includes the xyloglucan endotransglycosylase (XET). Both XEH and XET proteins are commonly grouped within the xyloglucan endotransglucosylase/hydrolase family (XTH) due to some of their members (like β‐xylanase) that can have both GH and GT activities [30].
Polysaccharide lyases (PLs) promote cell separation by calcium‐dependent de‐polymerization of wall polygalacturonides. Plant pectate lyases are a group of enzymes that catalyze the cleavage of de‐methylesterified pectin. PL activity has being described in cell wall degradation that occurs during fruit ripening [45], and Penfield et al. [7] report 34 pectate lyases that were downregulated in the endosperm of
Carbohydrate esterases (CEs) include two enzyme families that have activity over pectins, the PMEs and pectin acetylesterases (PAEs), and the family of xylan acetylesterases. These enzymes cleave methyl or acetyl groups from the HG or Xyl backbone of polysaccharides [30].
PMEs catalyze the reaction by which methylesters are cleaved from a HG chain, producing a free carboxyl group and the release of a proton and methanol [46]. Plant PMEs are mainly alkaline isoforms bound to the wall matrix, while some isoforms are neutral and easily solubilized or free apoplastic acidic isoforms. Alkaline isoforms seem to be the PMEs with most de‐methylesterification activity, but the kinetics of PME activity is affected by the ionic composition of the matrix, thus influencing PME activity and mobility [47]. PME activity can lead to two different cell wall fates: the first one would be the formation of a rigid, stable structure by Ca2+ interaction with de‐methylesterified GalA residues (>10) in the HG chains. The second fate of HG would be their degradation by polygalacturonases, where only small stretches or individual GalA residues are de‐methylesterified, thus leading to a more relaxed matrix [28, 46]. Also, PME activity acidifies the cell wall; this acidification would allow expansin activity (“acid grow”) [5]. PMEs are antagonistically regulated in the cell wall by proteinaceous PME inhibitors (PMEIs) meanwhile PGs by PG inhibitors (PGIPs) [28].
Expansins regulate cell wall loosening in a pH‐dependent manner by disruption of the hydrogen bonds between xyloglucans and cellulose. Sequence analysis indicates that expansins contain an N‐terminal domain slightly similar to the catalytic domain of the family‐45 endoglucanases; however no catalytic activity has been reported.
In
3.3. Cell wall modification
The molecular modification of the wall network can result in the relaxation of wall stress or “wall loosening” by the controlled rearrangement of cellulose/matrix polymers, which involve sliding of a cross‐link along a scaffold or the breakage of stress‐bearing cross‐links without substantial changes in wall dimensions. These rearrangements could include three processes: (a) the cleavage of the backbone of major matrix polymers, (b) the weakening of the non‐covalent bonding between polysaccharides, and (c) the breakage of cross‐links [5]. Following cell wall loosening, there are three main types of outcomes: cell expansion, cell separation, and wall stiffening. Cell wall enlargement occurs secondarily as a result of water uptake and the reduction of turgor pressure resulting from wall loosening [44].
Reactive oxygen species (ROS) like hydrogen peroxide (H2O2), hydroxyl radical (·OH), and superoxide radical (O2—) have been proposed to play a major role in germination by participating in defense against pathogens, signaling, and promotion of cell wall loosening [2, 9]. ROS can negatively affect germination by reacting with almost all macromolecules stored in the seed, causing oxidative damage and cleavage of polysaccharide chains in the cell walls [5, 9]. The participation of ROS in cell wall loosening and promotion of germination might be indirect, through the ethylene signaling pathways that involve ROS production and downstream activation of CWMPs [9]. Cosgrove [5] suggests the revision of ROS participation in the process of wall loosening, since in most studies reporting ROS‐mediated extensibility comprises only a small fraction (about 1% extensibility) and the assays with higher ROS concentrations provoke wall breakage.
3.4. Role and regulation of cell wall enzymes and proteins during germination
The study of plant cell wall structure and physiology has achieved a major progress from the input of “‐omics” technologies in the past two decades. These ‐omics technologies are able to capture the complexity of biological processes, like seed germination and cell wall modification, with high sensitivity and spatial‐temporal resolution. A tissue‐specific transcriptome analysis in
Cell wall modification can occur at five different stages during seed germination: (a) during the cellular expansion process triggered by rehydration of tissues, (b) at the onset of testa rupture, (c) during endosperm weakening and rupture, (d) during cellular expansion related to radicle elongation, and (e) during wall degradation and mobilization of stored reserves in both living and nonliving storage tissues.
3.4.1. Rehydration‐driven cellular expansion
Seed imbibition is given by the difference in water potential between the seed and the environment. Nonviable seeds swell faster than viable seeds, as viable seeds develop turgor pressure that restricts further water uptake [2]. However, rapid imbibition can still occur and lead to solute leakage and damage of membranes. Gradual rehydration of seed tissues has been detected in legumes like peas and beans, where hydration starts in the tissues near to the micropyle. As water diffuses in the outermost tissues, a waterfront is formed between imbibed tissues and those about to be imbibed. The testa plays a significant role in modulating imbibition kinetics and the waterfront formation [2]. The seeds of mutants with altered testa structure or altered deposition of protecting substances (like flavonoids, cutin, suberin, and lignin) have increased permeability and lower longevity than the wild type [52]. Testa structure usually consists of several layers of highly compressed dead cells where protective substances are deposited during seed development and maturation. Plant cell walls of living cells can also function as an interface that modulates water intake by changing wall porosity, thus allowing a gradual swelling of all tissues. This regulation could be achieved by rapid changes in wall extensibility as the ones generated by expansins. In support of this view, in whole unstratified
In many species from the Brassicaceae, Solanaceae, Linaceae, and Plantaginaceae, among others, the epidermis of the testa contains specialized cells that accumulate abundant pectins and heteroxylans, as well as some xyloglucans or arabinans during seed development. Upon imbibition these polysaccharides expand and burst out of the testa, generating a gel‐like structure. This phenomenon, known as myxospermy, has been used as a model to study several hydrolases and PME activity [54, 55]. Although there is still uncertainty about the actual role of myxospermy, the proposed roles include regulating hydration, preventing desiccation, being an oxygen barrier, or allowing the seed to attach to the substrate and animals [54–56].
3.4.2. Testa rupture
In many plant species, testa rupture starts at the micropylar seed end. In tobacco (
The seed testa is composed of several layers of nonliving cells, and thus the regulation and enzymes that facilitate cell separation in the testa must come from the living tissues underneath. At the onset of testa rupture (∼25 HAI), it is possible to identify 90 cell wall‐related genes from the 501 upregulated genes (∼18%) in the micropylar endosperm and 58 from 282 genes (∼20%) upregulated in the radicle. Also, about 8 (∼8%) and 5 (∼4%) genes were downregulated in both tissues, respectively [17]. In
Endosperm (HAI) | RA | Endosperm (HAI) | RA | ||||||||||||
---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|
Function | Gene ID | TS | 0–12 | 16 | 25 | 31 | 25 | Function | Gene ID | TS | 0–12 | 16 | 25 | 31 | 25 |
EXPA10 | AT1G26770 | No | 6–12 | 24 | TR* | β‐Gal | AT1G45130 | EM | Not specified | ||||||
EXPA1 | AT1G69530 | No | 3 | TR* | β‐Gal | AT5G08380 | No | Not specified | |||||||
EXPA15 | AT2G03090 | No | 12 | 24 | TR* | β‐Gal | AT1G77410 | EN | 24 | 31c | |||||
EXPA6 | AT2G28950 | EM | TR | β‐Gal | AT2G28470 | No | 16c | 24 | 24 | ||||||
EXPA4 | AT2G39700 | No | 16 | β‐Gal | AT4G26140 | No | 31 | ||||||||
EXPA2 | At5g05290 | No | 3 | 24 | β‐Glu | AT1G61820 | EN | Not specified | |||||||
EXPA8 | At2g40610 | No | 3–12 | 24 | β‐Glu | AT1G70710 | No | 16 | TR* | ||||||
EXPA3 | At2g37640 | No | 6–12 | 24 | β‐Glu | AT4G16260 | EN | Not specified | |||||||
EXPA9 | AT5G02260 | No | 12 | 24 | β‐Glu | AT1G26560 | EM | Not specified | |||||||
EXPA20 | AT4G38210 | No | 6–12 | 24 | β‐Glu | AT3G62750 | No | 3c | |||||||
EXPB1 | At2g20750 | No | 12 | β‐Glu | AT2G44450 | No | TR | 31 | |||||||
EXLA3 | AT3G45960 | No | TR | β‐Glu | AT4G34480 | No | 12* | ||||||||
EXLA1 | AT3G45970 | No | 16 | TR | TR | MAN5 | AT4G28320 | No | Not specified | ||||||
EXLA2 | AT4G38400 | No | 6–12* | TR | TR | MAN6 | AT5G01930 | EN | Not specified | ||||||
EXT3 | AT1G21310 | EM | Not specified | MAN7 | AT5G66460 | No | 6 | 24 | |||||||
EXT10 | AT5G06640 | EM | Not specified | GH | AT5G49360 | EN | TR | ||||||||
EXTL | AT3G54590 | EM | Not specified | GH | AT5G57560 | No | 16 | TR | |||||||
EXTL | AT4G38770 | EM | Not specified | GH | AT5G08370 | No | 16c | TR | 31c | ||||||
EXTL | AT2G27380 | RA | Not specified | GH | AT3G55430 | No | TR | 31 | 24* | ||||||
XTH5 | AT5G13870 | No | 6 | 24 | 24 | GH | AT3G07320 | No | 24 | 31 | 24 | ||||
XTH33 | AT1G10550 | No | 12 | 16 | TR | TR | GT | AT3G10320 | EN | 31c | |||||
XTH | AT1G11545 | No | 16 | TR | GH | AT3G13790 | No | 16 | 31 | ||||||
XTH | AT1G32170 | No | TR | GH | AT5G64570 | No | 24 | TR | |||||||
XTH17 | AT1G65310 | No | TR | GH‐DUF3357 | AT1G12240 | No | 31 | TR | |||||||
XTH | AT2G06850 | No | 16 | TR | 31 | TR | GH | AT3G47010 | EN | 24 | |||||
XTH | AT2G36870 | No | 31 | KOR2 | AT1G65610 | No | 31 | ||||||||
XTH | AT3G23730 | No | TR | TR | CESA5 | AT5G09870 | No | TR | 31 | 24 | |||||
XTH11 | AT3G48580 | No | 16 | 24* | 31 | CSLC | AT4G07960 | No | TR | TR | |||||
XTH | AT4G03210 | No | TR | TR | AGP | AT3G11700 | No | TR | TR | ||||||
XTH | AT4G14130 | No | TR | TR | AGP | AT5G44130 | EN | TR | |||||||
XTH24 | AT4G30270 | EN | 16 | TR | TR | AGP | AT1G28290 | No | 16 | 31 | |||||
XTH18 | AT4G30280 | No | 16 | TR | TR | PRT | AT3G54400 | No | 16 | 24 | |||||
XTH | AT4G30290 | No | 16 | 31 | PRT | AT3G61820 | No | TR* | 31 | 24 | |||||
XTH | AT4G37800 | EM | Not specified | PRT | AT4G16563 | No | TR | TR | |||||||
XTH25 | AT5G57550 | No | 6* | TR | TR | PL | AT3G24670 | EM | 24 | ||||||
XTR8 | AT3G44990 | EN | 16c | 24 | PL | AT3G27400 | No | TR | 24 | ||||||
XTR6 | AT4G25810 | No | TR | TR | PL | AT4G13710 | EN | Not specified | |||||||
PL | AT4G24780 | No | TR* | PMEI | AT5G20740 | No | TR | TR | |||||||
PL | AT5G48900 | EM | Not specified | PMEI | AT5G46940 | EN | TR | ||||||||
PX | AT1G14540 | EN | TR | PMEI | AT5G62340 | No | 16 | TR | |||||||
PX | AT1G14550 | EN | Not specified | PMEI | AT5G64620 | No | 31c | ||||||||
PX | AT1G30870 | EM | Not specified | PG | AT3G59850 | No | 16 | TR* | 31 | ||||||
PX | AT2G18980 | No | TR | 31 | PG | AT3G61490 | EM | Not specified | 24 | ||||||
PX | AT2G43480 | RA | Not specified | PG | AT4G23820 | No | 12 | TR | 24 | ||||||
PX | AT3G01190 | EM | Not specified | Kinase | AT1G33590 | No | TR | 31 | TR | ||||||
PX | AT3G21770 | EN | 31c | Kinase | AT2G23770 | No | TR | ||||||||
PX | AT3G28200 | No | TR | 31 | Kinase‐DUF26 | AT3G22060 | MI | 16 | 31 | ||||||
PX | AT4G08770 | EM | Not specified | Kinase | AT1G51940 | No | TR | TR | |||||||
PX | AT4G31760 | EM | Not specified | LRR‐p | AT4G26690 | No | TR | TR | |||||||
PX | AT5G05340 | No | 31 | LRR‐p | AT5G16590 | No | 16 | TR | 31 | TR | |||||
PX | AT5G39580 | No | 3 | TR | LRR‐p | AT2G34930 | No | 16 | TR | 31 | TR | ||||
PX | AT5G40150 | EM | Not specified | DUF642 | AT1G80240 | EM | Not specified | ||||||||
PX | AT5G64100 | No | 16 | TR | 31 | DUF642 | AT2G34510 | EM | Not specified | ||||||
PX | AT5G64120 | EN | TR | 31 | DUF642 | AT2G41800 | RA | Not specified | |||||||
PME | AT3G14310 | No | 6–12 | 24 | 24 | DUF642 | AT3G08030 | No | 3 | 31 | |||||
PME | AT1G04680 | No | 31 | TR | DUF642 | AT4G32460 | No | 16 | 31 | ||||||
PME | AT1G57590 | EM | Not specified | 24 | DUF642 | AT5G11420 | No | 3 | 31 | ||||||
PME | AT3G09410 | EM | Not specified | DUF642 | AT5G14150 | EM | Not specified | ||||||||
PME | AT3G10720 | No | 16 | TR | 31 | TR | OX | AT1G62380 | No | 16c | |||||
PME | AT3G62060 | EM | Not specified | 24 | OX | AT1G76160 | No | TR | |||||||
PME | AT4G19420 | EN | Not specified | OX | AT2G46740 | EN | 16 | TR | 31 | ||||||
PME | AT5G26670 | RA | Not specified | OX | AT4G22010 | No | TR | ||||||||
PME | AT5G45280 | No | 3 | 31 | OX | AT4G38420 | No | TR | TR | ||||||
PME | AT5G62330 | EM | Not specified | 24 | OX | AT5G21105 | No | 16 | TR | 31 | |||||
PME2 | AT1G02810 | No | 12 | 16 | 31 | OX | AT5G44380 | No | TR | 31 | |||||
PME2 | AT1G11580 | No | 16 | 24 | PTRI | AT1G17860 | No | TR | 31 | TR | |||||
PME2 | AT2G26440 | No | 16 | 31 | 24 | PTRI | AT2G38870 | No | 31 | TR | |||||
PME2 | AT3G47400 | No | 31 | 24 | PTRI | AT4G22470 | MI | TR | 31 | ||||||
PME2 | AT3G49220 | No | TR | TR | GT | AT1G64390 | No | 16 | TR* | 31 | |||||
PME2 | AT4G02330 | No | 16 | TR | 31 | TR | GT | AT2G02990 | EN | TR | |||||
PME2 | AT4G33220 | EM | Not specified | GT | AT2G14610 | EN | Not specified | ||||||||
PME2 | AT5G64640 | EM | 12 | 24 | GT | AT1G05170 | EM | TR* | |||||||
PMEI | AT1G62770 | RA | Not specified | GT | AT1G08280 | No | 31 | ||||||||
PMEI | AT2G47670 | EM | 3‐12* | 24* | PGIP | AT5G06860 | No | TR | |||||||
PMEI | AT4G00080 | No | 31 | TR | PG | AT2G43860 | MI | 24 | 31 | ||||||
PMEI | AT4G12390 | EM | Not specified | PG | AT3G06770 | No | TR | 24 |
In
In non‐endospermic seeds, testa rupture marks the end of germination. In this type of seeds, the testa rupture is accompanied by radicle elongation whose continued pressure in the inner face of the testa promotes cell separation [53].
3.4.3. Endosperm weakening for radicle protrusion
The endosperm functions as a barrier to control radicle protrusion as it can impose primary dormancy in many species like
The hydrolytic activity of β‐glucanases or endo‐β‐mannanases can contribute to endosperm cell wall weakening in Brassicaceae and Solanaceae species, which have cell walls rich in mannans [59]. In
Several reports indicate that endosperm weakening and rupture are inhibited or delayed by ABA, in a dose‐dependent manner, in some species of the Brassicaceae family [8, 16] and tobacco [63]. Microarray analysis of
3.4.4. Embryonic axis elongation
Cell elongation, rather than cellular division, is the main process that drives embryo growth [14]. Cell division occurs after radicle protrusion and contributes to the rapid growth of the embryonic axis by generating new elongating cells [2]. Cell elongation that drives radicle protrusion occurs at the transition zone, which comprises the cells between the last proximal root hair cell in the radicle and the lower basal cells of the hypocotyl [69]. In
In the micropylar endosperm of tomato seeds, an important mobilization of protein bodies occurs, but it seems that there is no cell degradation as the radicle protrudes. Instead, a process similar to cell separation to allow radical protrusion was suggested [70]. A similar process was observed in celery seeds, where the radicle tip also seems to penetrate the micropylar endosperm by separating the endosperm cells, but, since the embryo needs to grow before germination is completed, cell degradation for storage mobilization occurs in the endosperm adjacent to the embryo [27]. The expression of
3.4.5. Cell wall participation in the mobilization of stored reserves
Major reserve mobilization occurs once germination has concluded, and these reserves are utilized to feed the growing seedling rather than to fuel radicle protrusion. However, in cereal grains, the preparation for starch and oligosaccharide mobilization occurs within the first hours of germination [15]. In cereals, the endosperm is a nonliving storage tissue, and the endosperm cell walls protect its contents from enzymatic attack. Accordingly, the degradation of cell walls is a limiting step in storage reserve mobilization that is induced by the GA produced by the embryo (at the scutellum) and secreted to the aleurone layer [2].
In most endospermic seeds this tissue is still living. Mannans in the endosperm cell walls of date palm (
4. Concluding remarks
In‐depth temporal screening of cell wall‐related transcripts and proteins has provided an important overview of the possible actors involved in the five stages during germination where wall modification is involved, as described above. In
Spatial transcriptomic analyses that include the different seed compartments and the analysis of cell wall composition changes using specific antibodies for in situ localization of the different polysaccharide epitopes in seed tissues provide valuable information. Although
ROS participation in germination is supported by several reports and transcriptomic profiles of germinating seeds [9, 14, 17]. However, the actual role of ROS and ROS‐related enzymes in promoting cell wall loosening needs to be further analyzed, since the physiological concentrations of ROS during germination do not seem to be sufficient to induce wall extension, and attempts of increasing ROS concentration lead to wall breakage [5]. Müller et al. [72] describe abnormal rupture of the micropylar endosperm of
Acknowledgments
This work was supported by Programa de Apoyo a Proyectos de Investigación e Innovación Tecnológica (PAPIIT) IN207915 and SEP‐CONACyT grant 155074. Ximena Gómez‐Maqueo acknowledges the scholarship by the Consejo Nacional de Ciencia y Tecnología (CONACyT).
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