pollen germination and tube growth - Annual Reviews

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ABSTRACT. Many aspects of Angiosperm pollen germination and tube growth are discussed including mechanisms of dehydration and rehydration, in vitro ...
TAYLORGERMINATION POLLEN & HEPLER Annu. Rev. Plant Physiol. Plant Mol. Biol. 1997. 48:461–91 Copyright © 1997 by Annual Reviews Inc. All rights reserved

POLLEN GERMINATION AND TUBE GROWTH Loverine P. Taylor Department of Genetics and Cell Biology, Washington State University, Pullman, Washington 99164-4234

Peter K. Hepler Biology Department, University of Massachusetts, Amherst, Massachusetts 01003 KEY WORDS: pollen germination, pollen tube, tip growth

ABSTRACT Many aspects of Angiosperm pollen germination and tube growth are discussed including mechanisms of dehydration and rehydration, in vitro germination, pollen coat compounds, the dynamic involvement of cytoskeletal elements (actin, microtubules), calcium ion fluxes, extracellular matrix elements (stylar arabinogalactan proteins), and control mechanisms of gene expression in dehydrating and germinating pollen. We focus on the recent developments in pollen biology that help us understand how the male gamete survives and accomplishes its successful delivery to the ovule of the sperm to effect sexual reproduction.

CONTENTS INTRODUCTION..................................................................................................................... IN VITRO GERMINATION .................................................................................................... DEHYDRATION AND HYDRATION ................................................................................... Water Loss and Phase Transition ....................................................................................... Imbibition............................................................................................................................. POLLEN COMPONENTS INVOLVED IN GERMINATION ............................................... Pollen Coat .......................................................................................................................... Waxes................................................................................................................................... Oleosins ............................................................................................................................... Flavonoids ........................................................................................................................... POLLEN TUBE GROWTH...................................................................................................... Overview of the Pollen Tube Structure ...............................................................................

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461 1040-2519/97/0601-0461$08.00

462 TAYLOR & HEPLER Actin Microfilaments ........................................................................................................... Actin-Binding Proteins ........................................................................................................ Microtubules........................................................................................................................ Calcium Ions........................................................................................................................ Extracellular Matrix Components....................................................................................... Pollen Wall and Pectin ........................................................................................................ Arabinogalactan Proteins ................................................................................................... Pulsatory and Oscillatory Growth ...................................................................................... GENE EXPRESSION DURING THE PROGAMIC PHASE.................................................. Translational Control .......................................................................................................... Translational Mechanisms in Dehydrated Pollen............................................................... Gene Expression During Pollen Germination and Tube Growth ....................................... Genes Involved in Pollen Metabolism.................................................................................

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INTRODUCTION Pollen develops within the anther and at maturity contains the products of sporophytic gene expression, arising from the tapetal layer of the anther wall, and gametophytic gene expression from the vegetative and generative nuclei. The progamic phase of development begins with pollen dehydration, a survival aid during dispersal. When a pollen grain falls on a receptive stigma, the stored RNA, protein, and bioactive small molecules allow rapid germination and outgrowth of a tube that penetrates and grows within the style. Experiencing the most rapid growth of any plant cell known, which is restricted exclusively to the tip of the tube, the pollen tubes eventually deposit the two sperm cells in the embryo sac where they fuse with the egg and central cell to form the zygote and endosperm. Understanding this critical developmental process is not only important in our efforts to decipher the basic mechanism of sexual reproduction in flowering plants but also has value for the potential manipulation of crop plant production. This review focuses on many aspects of pollen germination and tube growth beginning with dehydration and ending just before tube entry into the ovary. There have been many recent reviews on pollen development, but most have focused on special subjects. Heslop-Harrison (54) and Mascarenhas (100) reviewed this topic broadly; however, the subject is large and progress continues in several areas at a rapid pace, justifying the present effort. Nevertheless, space constraints have forced us to curtail expanded discussions on many points, and to greatly restrict the number of literature citations.

IN VITRO GERMINATION Pollen of most species will germinate and grow a tube when placed in a solution of calcium, boron, and an osmoticant. Although it provides a controlled experimental system, germination in vitro does not completely mimic

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growth in vivo. Even with highly optimized germination media (GM), in vitro tubes reach only 30–40% of in vivo lengths, and structural anomalies are frequently observed (125). In addition, the pollen of some species, e.g. Arabidopsis thaliana, does not germinate well in vitro no matter what conditions are used (123). If only a fraction of the viable grains produce a tube, the resulting studies do not provide an accurate reflection of “germinating” pollen. Even though it is not possible to duplicate the dynamic interaction between the pollen and the pistil, nevertheless in many species germination and tube growth are robust under experimentally defined conditions, rendering in vitro–based studies of relevance to the in vivo situation. The composition of the GM can dramatically affect pollen metabolism. Under osmotically equivalent conditions, PEG-based GM increased germination frequency and prevented tube bursting when compared to sucrose (e.g. 125). PEG is relatively inert metabolically and cannot enter cells (138), whereas sucrose and/or monosaccharides enter the pollen and augment the already high internal concentrations (61, 71). High sucrose levels in the GM may alter the permeability of the growing pollen tube, resulting in leaching of metabolites and ions into the media (27, 49, 138, 178). Sucrose also fuels ethanolic fermentation during in vitro growth accumulating to levels in the GM (100 mM) that may inhibit growth (12). Whether ethanol is produced during in vivo growth is unknown.

DEHYDRATION AND HYDRATION Water Loss and Phase Transition Dehydration, which usually occurs just before anthesis, induces a metabolically quiescent state that confers a tolerance to the environmental stresses encountered during dispersal by water, wind, insects, or animals and may be a necessary prerequisite for pollen viability and subsequent germination (89). When released from the anther, pollen is partially dehydrated, with water contents ranging from 6 to 60%; the degree of hydration is species-specific (72). Despite desiccation, pollen is viable if the structural changes that occur during dehydration are reversible upon rehydration. Therefore, the conditions under which water loss occurs can significantly affect the subsequent adhesion and germination of pollen (72, 89, 157). Given the importance of pollen as a germplasm source (24), considerable effort has been vested in identifying the cellular targets of dehydration (e.g. 148). Water is a major determinant of the structural integrity and stability of cellular membranes, and the loss of this barrier is a major cause of decreased

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pollen viability. During dehydration water becomes increasingly bound and reaches a transition point where the phospholipid structure changes from a lamellar or liquid crystalline form to a gel state (27). The temperature at which this transition occurs depends on the water content (27). If conditions are suboptimal when the gel state is formed, e.g. extreme fluctuation in temperature and humidity during the dispersal phase, irreversible membrane injury can occur (72, 133). Free radicals, which are formed more readily in the dehydrated state, also contribute to membrane damage (72, 124, 157). As water is removed it is replaced by molecules that protect cellular structures. In other dehydrating tissues, various molecules accumulate, e.g. trehalose in nematodes and yeast and the hydrophilic LEA proteins in dry seeds. Neither of these molecules has been identified in pollen, but conditions in mature pollen foster expression of Dc3, a lea-class gene involved in water stress responses. In transformed pollen the Dc3 promoter was activated at the latest state of pollen development (149) and supported a twofold higher level of expression than LAT52, a late pollen-specific gene that functions during tomato pollen hydration (113). Sucrose may function as a desiccation protectant in pollen, because dehydration survival was correlated to its concentration (61).

Imbibition Pollen hydration proceeds in a controlled manner characterized by distinct plateaus of increasing water content (13, 48, 180) and can begin in the anther before pollen release (180). Hydration plateaus can be detected in vitro: Prehydrated petunia pollen increased threefold in volume compared to a twofold increase when desiccated pollen was exposed directly to bulk water (48). This study also found that the more hydrated the grain initially, the larger the final volume. The osmoticum also influences water uptake; tube volume was greater on sucrose-based medium than on a PEG medium (178). The damaging effects of immediate exposure of the desiccated grain to bulk water are demonstrated by the increased osmotic potential, ion concentration (K+, NAD+, and H+) and enzyme activity in the GM upon addition of pollen (e.g. 27, 49). Presumably this “imbibitional damage” results from altered membrane integrity; this could be caused by incomplete or abnormal reconstitution of the lipid bilayer upon rapid hydration, possibly involving a transition from gel to liquid crystalline phase (27) or the persistence of patches of gel phase lipids in the hydrated state (72). One model of imbibitional damage predicts that the leakage can be completely eliminated by prehydrating pollen before exposing it to bulk water (27). This effectively lowers the transition

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point temperature so that the partially hydrated phospholipids are already in the liquid crystalline phase when rehydrated (24, 49, 61). Ultrastructural and physiological studies of pollen hydration in Brassica detected two distinct phases of hydration (33, 40, 59). During the initial phase, putative signals are reciprocally exchanged between pollen and stigma (33). The second phase proceeds with an invagination of the intine in the colpial zone (aperture where pollen tube will emerge) and formation of a “foot” of pollen coating that contacts the stigma papilla. This “foot” may differ chemically from the rest of the pollen coat because a cyclohexane wash removes the coating except in this region (40). Freeze-etch preparations show microchannels at the papilla-pollen boundary through which water may flow. Water moves from stigma to pollen grain but not between grains and requires protein synthesis (131). The area around the site of pollen tube emergence is rich in pectins, and one of the earliest visible alterations of macromolecules upon hydration is a loss of protein and pectic material from the length of the colpial slit (57). Upon emergence from the germination pore, the tube grows through the foot layer and penetrates the papilla cell (40), possibly utilizing an active cutinase that is located in the intine layer and translocated to the pollen tube tip upon germination (58).

POLLEN COMPONENTS INVOLVED IN GERMINATION Pollen Coat Surface molecules provide contact and initiate the signaling necessary for successful adhesion (dry stigmas) and germination (wet and dry stigmas). The pollen wall consists of two layers, the inner pectic-cellulosic and the outer, highly sculpted exine, composed of sporopollenin (168). In the later stages of pollen development the tapetal layer of the anther wall disintegrates, and the cellular contents are deposited onto the surface of the pollen grain forming the tryphine (or pollenkitt) layer. The composition of this material is highly heterogeneous and includes waxes, lipid droplets, small aromatic molecules, and proteins.

Waxes Several alleles of the epicuticular wax mutants (cer) of Arabidopsis (76) have an altered tryphine coating and impaired male fertility (1, 64, 123). Microscopic and biochemical analysis of cer6-2 pollen showed that an aberrant tryphine layer deposited during development visually disappeared by dehiscence (123). The mutant pollen failed to hydrate but stimulated callose deposi-

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tion in the underlying stigma cell, a sign of an incompatible pollination. cer6-2 pollen was viable and could germinate in vitro, an observation that was exploited to reverse the male sterility (MS) by pollinating at high humidity. Chemical analysis of the cer6-2 pollen coat showed that almost none of the C29 and C30 waxes characteristic of wild-type (WT) pollen was present, suggesting that long-chain alkanes (C29) may be the bioactive molecule (123). Not all cer mutants with altered male fertility lack a tryphine (1, 64, 123); cer3-2186 has a visually normal pollen coating but exhibits a strong MS phenotype (64). Thus subtle changes in tryphine composition may have dramatic consequences for fertility. The failure of the cer mutants to stimulate release of water from the stigma to the pollen is interpreted as evidence that lipids in the pollen coat are involved in the cell-cell recognition required for hydration. By microscopic observation, elements in the coat show limited mobility and thus may move from grain to grain (40). This movement could explain the mentor pollen rescue of the MS cer phenotype by WT pollen (64, 123). Some cer mutants are temperature sensitive and can be successfully pollinated at lower temperatures (18°C versus 25°C) (64). Temperature has a profound effect on lipid viscosity, which could in turn affect the mobility and/or accessibility of substances suspended or dissolved in the tryphine layer. An important issue is whether lipid-mediated hydration is specific to species with dry stigmas (or even more narrowly to the Brassicaceae) or whether some elements also operate in pollinations on wet stigmas.

Oleosins Oleosin-like proteins have been detected in the tryphine layer (127). In seeds oleosins are associated with oil bodies; a model based on the presumed secondary structure of the oleosin protein proposes that the highly conserved central hydrophobic domain penetrates the oil body and that the N- and C-termini interact on the surface to stabilize the structure (62). The predicted protein product of the tapetum-specific oleosin-like cDNAs have an identical central hydrophobic domain but differ significantly from the majority of seed oleosins in the C-terminal region (e.g. 62, 126, 127). cer mutants lacking a tryphine (cer6-2) do not accumulate oleosin-like proteins (122, 127). Other cer mutants, which have an abnormal tryphine (e.g. cer6-1), have reduced amounts (D Preuss, personal communication). Even though the structure of the oleosinlike proteins recovered from cyclohexane washes of Brassica pollen do not contain the hydrophobic domain (127), there appears to be a connection between tryphine lipids and tapetal oleosins. Further analysis of mutant tryphine

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coatings for the presence of oleosin-like proteins will be required to establish a relationship.

Flavonoids In addition to lipids and proteins, small aromatic molecules such as carotenoids, flavonoids, jasmonates, phenolic acids, brassinosteroids, and most of the classic phytohormones have been detected in pollen (73, 96, 134, 168). Of these compounds only flavonols, a specific class of flavonoid, have a demonstrated role in pollen germination (110, 174). Virtually all pollens accumulate flavonols, often to very high levels (168). By genetic analysis, pollen flavonols are sporophytic in origin; they are synthesized in the tapetum, released into the locule, and taken up and modified by the developing gametophyte (161, 171). Early suggestions that flavonols stimulated pollen tube growth were confirmed with the isolation of flavonol-deficient plants, of which several now exist (23, 110, 174; C Napoli, LP Taylor, personal communication). Flavonoldeficient plants are self-sterile because the pollen fails to germinate (110, 142) or produce a functional tube (120, 174). The reproductive defect is conditional and can be biochemically complemented by adding flavonols at pollination or by WT stigma exudate (142, 160, 174). The bioactive compound from the stigma exudate was identified as kaempferol, a flavonol aglycone (110, 160). An in vitro pollen rescue assay established that the response to exogenous flavonols was sensitive (0.4 µM), specific for flavonol aglycones (110, 162, 174) and rapid: Tube outgrowth occurs within 2 min (110). Although flavonols accumulate before pollen maturity (28, 120, 121), all the biochemical and histological evidence indicates that they function only at germination. Although the mechanism of flavonol action remains to be determined, a structural role within the cell wall (53) has been excluded by feeding studies using a radiolabeled flavonol (171); rather, it seems that flavonols may be localized to cytoplasmic compartments (173). Feeding experiments also showed that flavonols were not catabolized during germination but were rapidly (230) whose appearance is coincident with germination (101) suggests that it may be

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Table 1 Genes expressed in germinating pollen Gene/species

Function/ homology

Location

How determined

Reference

PAB5 A. thaliana

poly(A) binding protein

germinating pollen

Transgenic plant, GUS activity

9

tua1 A. thaliana

tubulin

germinating pollen

Transgenic plant, GUS activity

18

Bcp1 B. campestris

AGP-like

germinating pollen

Northern

144

Gs15 Glycine max

Glutamine synthase

germinating pollen

Transgenic lotus, GUS activity

97

CDPK maize

Ca+2-dependent protein kinase

germinating pollen

Northern, western and 41 antisense oligonucleotide suppression

pex1 maize

chimeric extensin-like

pollen tube wall, callose layer

Immunolocalization (FTIC and TEM)

129

PGc9 maize

polygalacturonase

pollen tube wall

Immunolocalization (FTIC); Transgenic plant (tobacco), GUS activity

37

W2247 maize

polygalacturonase

pollen tube tip

Transgenic plant (tobacco) 2, 143 and pollen bombardment, GUS activity

Zm13 maize

protease inhibitor/LAT52

vegetative cell cytoplasm

In situ hybridization

51

neIF-4A8 N. tabacum

RNA helicase

germinating pollen

Transgenic plants and pollen bombardment, GUS activity

11

NTP303 N. tabacum

ascorbate oxidase/LAT51, Bcp10

vegetative cell cytoplasm, tube tip

Northern; Pulse labelling

166

chiA (PA2) Petunia hybrida

chalcone isomerase

germinating pollen

Transgenic plants, GUS activity

158

PGP76 P. hybrida

leucine-rich repeat Cf-2, Cf-9

germinating pollen

Northern

V Guyon & LP Taylor, unpubl data

PGP177 P. hybrida

serine-rich

germinating pollen

Northern

V Guyon & LP Taylor, unpubl data

PGP 220 P. hybrida

AGP-like

germinating pollen

Northern

V Guyon & LP Taylor, unpubl data

ppe1 Petunia inflata

pectin esterase/ Bp19

pollen tubes

Northern

112

PRK1 P. inflata

receptor-like protein kinase

pollen tubes

Northern and western

111

Ps1 Rice

protease inhibitor/ LAT52/pZm13

potten tube

Northern; Transgenic plants, GUS activity

179

482 TAYLOR & HEPLER Table 1 (continued) Gene/species

Function/ homology

Location

How determined

Reference

LAT51 tomato

ascorbate oxidase/ Bp10/NTP303

tube tip and cytoplasm

In situ hybridization

153

LAT52 tomato

Kunitz trypsin inhibitor/pZm13

tube tip and cytoplasm vegetative cell nucleus

In sity hybridization transgenic plant, nuclear targeted GUS activity

151, 153

LAT56 tomato

pectate lyase/ LAT59/TP10/ Zm58

tube tip and cytoplasm

In situ hybridization tissue print

31, 153

LAT58 tomato

None

tube tip and cytoplasm

In situ hybridization

153

LAT59 tomato

pectate lyase/ LAT56/TP10/ Zm58

tube tip and cytoplasm

In situ hybridization

153

premature to conclude that none of them arises from transcripts activated specifically at germination. Some early gene products such as alcohol dehydrogenase, actin (99), and a heat-shock protein cognate from tomato (38) persist in germinating pollen. The issue of protein turnover must be examined in parallel with the posttranscriptional control of pollen gene expression. Ubiquitin-mediated protein degradation has not been demonstrated in pollen, although elements of the system are present in virtually all gymnosperm and angiosperm pollens examined (78). Some maize inbreds show a progressive loss of ubiquitin and ubiquitinated conjugates during pollen maturation (16), but the significance of this for pollen development is unclear because it is not shown by the vast majority of species (78). LATE GENES Although the late genes are transcriptionally activated before dehydration, their persistence during germination and growth argues for a functional role at this stage (see Table 1). Because of the method of isolation, most of the genes in Table 1 represent abundant transcripts, and currently their function in pollen tube growth is predicated on the shared homology with genes of known function (103, 152, 173). Some sequences defy classification because they have no homology to known genes, and others may serve multiple functions as suggested by differential localization (e.g. Pex1, PG) and/or expression (e.g. Bcp1) before and after germination. KINASE SEQUENCES IN POLLEN TUBES A pollen-specific calcium-dependent calmodulin-independent protein kinase (CDPK) isolated from maize suggests

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the presence of posttranslational control mechanisms involving Ca2+ and phosphorylation (41). The gene is transcribed in mature and germinating pollen and is required for germination. When antisense oligonucleotides to the kinase sequences were added to the GM, germination was abolished or severely diminished. The same effect was seen if an antagonist of calmodulin or a CDPK inhibitor was present at germination. Transcripts to a receptor-like serinethreonine protein kinase, PRK1, were detected for at least 16 h after pollen germination in petunia (111). Although PRK1 was isolated from germinating pollen, transgenic plants expressing the cDNA in an antisense orientation showed arrested pollen development at the uninucleate microspore stage (84). Because the premature pollen abortion precluded testing a role in germination, another approach, perhaps the use of antisense PRK1 oligonucleotides at germination, will be necessary. If PRK1 functions at two different stages it will be interesting to know whether the kinase substrates are identical in developing and in germinating pollen.

Genes Involved in Pollen Metabolism Some genes are expressed in both the sporophyte and the gametophyte, usually at different times in development (e.g. 144). Bcp1 was expressed in the tapetum of Brassica campestris anthers and in germinating pollen up to 5 h postgermination (144). Promoter analysis of Bcp1 showed that tapetal and pollen expression were controlled by different regulatory sequences (170) and that perturbation of expression in the tapetum resulted in plants that aborted all pollen at the late uninuclear stage. To test the role of Bcp1 expression in pollen, an antisense copy of the cDNA was expressed from the pollen-specific LAT52 promoter from tomato. Bcp1 expression was not perturbed in the tapetum of these plants, but 50% of the pollen aborted at the bicellular stage (170). Thus expression of Bcp1 is required in both sporophyte and gametophyte with the tapetal requirement preceding the pollen. The most complete analysis of transcription during pollen germination is that of the NTP303 gene from N. tabacum. Northern analysis and pulse-labeling of in vitro–germinated pollen detected transcripts at 10 h but not 20 h after germination (166). However, subsequent analysis by in situ hybridization detected NTP303 transcripts in pollen tubes growing for 72 h in the stylar transmitting tract. By this time, the tube had reached the ovary. The RNA was localized to the vegetative cell and to the tip of pollen tube (167). In situ hybridization and immunocytochemical techniques showed that pectin-degrading polygalacturonase (PG) is differentially localized, being present in the cytoplasm of ungerminated grains and in the wall of the elongating tube (e.g.

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2, 37). Expression in germinating pollen was confirmed in both stably and transiently transformed pollen expressing a PG promoter-GUS marker gene fusion (37, 143). The resolution of in situ hybridization does not allow the detection of any contribution to this signal by the relatively small generative cell. To demonstrate cell-specific transcriptional activation of a GUS reporter gene, Twell et al (151, 152) added a nuclear targeting sequence to the LAT52 GUS construct. Transgenic plants expressing GUS activity showed staining only in the vegetative nucleus, confirming that the LAT52 promoter was active only in the vegetative cell. The construct was subsequently used to show vegetative-cellspecific expression of LAT52 in tricellular pollen (Arabidopsis), although in this instance it was activated before PMI rather than after, as in bicellular pollen (39, 152). LAT52 is a well-characterized example of a late pollen gene. It is expressed from PMI onward, and transcripts have been detected after 18 h of in vitro germination (113, 153). LAT52 has sequence homology to genes encoding proteinase inhibitor proteins, but the activity of the expressed protein has not been determined (113). To define a role for LAT52 in pollen function, antisense LAT52 tomato plants were analyzed. Segregation analysis of two classes of the transgenic plants confirmed that LAT expression was required for viable pollen (113). Primary transformants with reduced LAT52 mRNA and protein levels developed normally and showed no pollen abnormalities until the hydration phase. The transgenic grains did not appear to imbibe water from a PEG-based GM but hydrated normally when placed in an aqueous solution without PEG. The water flux was reversible because the abnormal shape was reconstituted by placing the hydrated pollen in PEG media. The mediating effect of PEG on the mutant phenotype may be related to its known effect on slowing water uptake (150). More importantly, the mutant phenotype was expressed when the pollen was hydrated on the stigma: In vivo pollination showed that many grains did not germinate and those that did grew knotted and twisted pollen tubes. ACKNOWLEDGMENTS We thank members of the plant reproductive community as well as members of the Taylor and Hepler research groups who were generous with their time for helpful discussions. The authors research presented in this review was supported by grants USDA NRICGP 9337304-9435 and NSF IBN-9405361 to LPT and NSF MCB-9304953 and MCB-9601087 to PKH.

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