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Ovary Signals for Directional Pollen Tube Growth

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Ovary Signals for Directional Pollen Tube Growth Sex Plant Reprod (2001) 14:3–7 © Springer-Verlag 2001 REVIEW M. Herrero Ovary signals for directional pollen tube growth Received: 15 December 2000 / Accepted: 13 June 2001 Abstract In angiosperms, the female gametophyte has a work has focussed on pollen tube growth along the stig- secluded life; it is protected by several concentric layers ma and style, the ovary has been neglected; it has often that envelop each other. The embryo sac is surrounded been assumed that once the pollen tubes arrive at the by the nucellus, which in turn is wrapped by the integu- base of the style fertilisation occurs. However, informa- ments forming the ovule, which is nested in the ovary. tion is converging toward the concept (Herrero 2000) These wrappings are not hermetic, but contain little that the process is far from straightforward, and that in “gates” the pollen tube must traverse on its way towards the ovary, also, an interesting male-female interaction the embryo sac. Information is emerging that shows that occurs. the ovary and ovule provide signals orienting and direct- A close look at the ovary shows that the female game- imng the pollen tube on the right course. There are three tophyte has a secluded life, protected by a number of main bodies of evidence supporting this hypothesis. One concentric layers that consecutively envelop each other. relates to developmental changes in the female tissues Thus, the embryo sac is surrounded by the nucellus, and how they affect pollen tube growth. The second re- which in turn is wrapped by the integuments forming the fers to defective ovule mutants, which induce defective ovule, which is nested in the ovary. These structures are pollen tube guidance. And the third relates to the possi- highly conserved in flowering plants, and in spite of ear- ble molecules involved in this signalling. Here, informa- ly descriptions little attention has been devoted to their tion gathered along these three main lines of evidence is possible role. It is assumed that they have a protective reviewed. All converge to the conclusion that different function, first of the embryo sac and later of the develop- checkpoints exist all along the pollen tube pathway. ing embryo. However, these wrappings are not hermetic; These checkpoints provide active signalling that guides they provide little “gates” the pollen tube must traverse the pollen tube to its destination, the embryo sac. on its way toward the female gamete. The pollen tube pathway in the ovary has been described in a number of Keywords Ovary · Ovule · Embryo sac · Pollen tube species, but there is little evidence showing how this trail growth is blazed. Information is emerging that indicates the ova- ry and the ovule provide signals that orient and direct the pollen tube to set the right course. There are three main Introduction bodies of evidence supporting this point. One relates to developmental changes in the female tissues and how The pistil is a clear stage for male-female interaction they affect pollen tube growth. The second refers to de- (Knox 1984). It plays a significant role in controlling fective ovule mutants, which induce defective pollen pollen tube growth (Linskens 1986; Mascarenhas 1993), tube guidance. Finally, the third relates to the possible fostering self-incompatibility mechanisms (Heslop- molecules involved in this signalling. Here, information Harrison 1983; Dickinson 1995) and favouring pollen gathered about these three main lines of evidence is re- competition and selection (Mulcahy 1979). Also, the en- viewed. tire pistil has been viewed as having a protective and prophylactic role (Heslop-Harrison 2000). While most Developmental changes in the ovary M. Herrero and ovule play a part in pollen tube guidance Unidad de Fruticultura, SIA-DGA, Campus de Aula Dei, Apartado 727, 50080 Zaragoza, Spain e-mail: [email protected] The idea that particular developmental stages have to be Fax: +34-976-716335 attained before the pistil is competent to receive the male 4 gametophyte appears to be universal in the reproductive number of different species (for reviews see Tilton 1980 process. Once the pollen grain germinates at the stigma and Sage et al. 1994). Little is known about the possible and the pollen tube reaches the base of the style, the pol- functions of this secretion, although it is tacitly assumed len tube tip alights on the placental surface and crawls that, somehow, it is needed for pollen tube growth. on its surface until it eventually turns towards an ovule, While these changes occur in the sporophytic tissues, penetrates the ovule and achieves fertilisation. In some the megagametophyte itself also plays a role in pollen species and circumstances, pollen tube growth proceeds tube growth. Little is known about changes in the em- smoothly. In these cases, although changes can be ob- bryo sac and how they relate to pollen tube penetration, served in the pistil tissues, it is difficult to establish the but the main candidate as signal provider for pollen tube influence that these changes have on pollen tube growth. penetration is the synergid. While the precise role syner- But, in other instances, accelerations and decelerations gids play is still to be discovered, it is apparent that they of pollen tube growth occur along this path (Herrero and are involved in pollen tube penetration to the embryo Arbeloa 1989). Furthermore, in some instances pollen sac, since the pollen tube consistently enters through a tubes navigate in a chaotic way, lose direction and do not synergid (Jensen 1965). In addition, experiments with in achieve fertilisation (Herrero 2000). These apparently vitro fertilisation have shown that pollen tubes do not abnormal situations provide a useful tool for detecting arrive at embryo sacs containing disrupted synergids what is happening in the pistil and how these changes re- (Higashiyama et al. 1998). Likewise, the presence of a late to pollen tube behaviour. complete egg apparatus appears to be a requisite for pol- Information is accumulating that shows there is not a len tube attraction (Shimizu and Okada 2000). As the single “checkpoint”, but that several structures all along synergid degenerates, two actin coronas develop, one at the pollen tube pathway are involved in pollen tube regu- the chalazal end of the degenerating synergid and anoth- lation. So far, evidence is dispersed and fragmented, il- er at the interface between the egg cell and central cell. lustrating different cases in different species. The placen- The formation of these coronas is concomitant with pol- ta often has little bumps that face the ovules physically len tube arrival and appears to be required for effective directing the pollen tube to the ovule entrance (the exos- migration of the sperm cells towards the egg cell and po- tome). In some species these bumps are called obtura- lar nucleus to achieve double fertilisation. (Huang and tors. The term was described early (Juel 1918) and Russell 1994; Russell 1996). reported in a number of unrelated species (Tilton and Thus, developmental changes occur all along the pol- Horner 1980). In these species the pollen tubes consis- len tube pathway in the ovary. All of this dispersed infor- tently traverse along the obturators to reach the ovules. mation appears to share a common idea, and this is that In peach (Prunus persica), the obturator, far from being events occurring along with pistil developments have a a passive structure, plays a clear part in regulating pollen bearing on pollen tube development. tube access to the ovule. When the pollen tubes arrive at the obturator, growth is arrested and does not resume un- til some 5 days later, when the obturator enters a secreto- Mutants with distorted pollen tube guidance ry phase (Arbeloa and Herrero 1987). Interestingly, in ki- wi (Actinidia deliciosa), a species where smooth and While the developmental approach shows that time plays rapid pollen tube growth occurs, obturators also lie along a major role in pollentube growth and that for successful the placenta, one facing each ovule. However, in this fertilisation male-female synchronism is required, defec- species a secretion is present in the obturators right from tive mutants provide a genetic dissection of the process- anthesis and the pollen tubes swiftly grow along on them es involved. Analysis of defective mutants which have to reach the ovules (Gonzalez et al. 1996). In Zea mays, reduced fertility due to failures in pollen tube guidance is a similar mechanism has been described. Papillar hairs an incipient field. However, it is surely going to clarify cover the ovary entrance. As the pollen tubes pass by, how the reproductive process is controlled, and also these hairs lose turgidity and prevent other pollen tubes which genes play clear roles in species isolation. The from entering the ovary (Heslop-Harrison et al. 1985). first evidence showing that a normal megagametophyte These mechanisms appear to act as drawbridges regulat- was required for directional pollen tube growth came ing pollen tube access to the ovule at a particular time. through the use of defective mutants that failed to devel- Once the pollen tubes traverse the placenta and face op an embryo sac and also failed to attract the pollen the ovule, further control appears to be exerted; ovule tube (Hulskamp et al. 1995). However, since these mu- penetration appears to be a chemotropic response tants were sporophytic, it could not be ruled out that the (Mascarenhas 1978). In peach, it has been described that loss of pollen tube guidance was due to a defect in the in some ovules the pollen tubes wander around the ovule sporophytic tissue (Hulskamp et al. 1995; Drews et al. exostome, while in other ovules penetration occurs. Pol- 1998). To overcome this difficulty Ray et al.
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