Conserved features of germination and polarized cell growth: a few insights from a pollen-fern spore comparison

Abstract

Background: The germination of both pollen and fern spores results in the emergence of a cell-pollen tube from pollen, rhizoid from spore-that grows in a polar fashion, primarily at its apical end. In both of these tip-growing cells, the delivery of secretory vesicles to the growing end is guided in part by a calcium gradient, with calcium entering at the tip where it is most highly concentrated. The similarities between the two systems extend beyond tip-focused calcium gradients to encompass signalling pathways and elements including calmodulin, nitric oxide, annexins and Rop-GTPases.

Scope and aims: This review is limited to those pathways and elements that function similarly in fern and pollen systems based on currently available evidence. The aim is to illustrate the common mechanisms by which tip growth occurs, facilitate further investigations into this area, and examine the implications for the evolutionarily conserved control of tip growth.

Conclusions: The interplay of calcium, nitric oxide and other effectors in both pollen and fern spores suggests certain signalling pathways became important regulators of germination and growth early in the evolution of land plants. Both large- and small-scale comparative genomic methods have shown to be promising in their ability to find new and relevant comparisons for further research. Cross-species comparisons may serve to speed up this process by highlighting both basic pathways and system-specific deviations.

Fig. 1.

Visualization of calcium gradients and annexin localization in germinating spores and growing Nicotiana pollen tubes. Pseudo-coloured images of spores and pollen tubes as visualized with the calcium indicator dye fura-2 (A, C) or FITC fluorescently labelled secondary antibodies against p35 annexin (B, D). Since different colour scales were used in each case, arrows indicate the areas of highest tip-related signal intensities. (A) Germinating Dryopteris spore loaded with fura-2. The yellow spot on the right indicates high levels of Ca²⁺ at the primary rhizoid initial. From R. Scheuerlein, M. Poenie, G.B. Clark et al., University of Texas at Austin, Austin, USA, unpubl. res. (B) Immunofluorescent localization of annexins in a germinating Anemia spore. In this colour scheme, the darker region within the yellow spot indicates highest immunoflourescent signal and corresponds to the rhizoid initial. Intense signal at the rhizoid tip is seen in longer rhizoids as well. From Clark et al. (1995) with permission from Springer Berlin/Heidelberg. (C) Nicotiana pollen tube loaded with fura-2-dextran. The red and white colours at the tip indicate high levels of Ca²⁺. Reprinted from Developmental Biology, 174, Pierson ES, Miller DD, Callaham DA, Van Aken J, Hackett G and Hepler PK, Tip-localized entry fluctuates during pollen tube growth, Pages 160–178, Copyright (1966), with permission from Elsevier. (D) Immunolocalization of annexins in a Nicotiana pollen tube. The dark area at the tip indicates the highest fluorescent signal. From R. Scheuerlein, M. Poenie, G.B. Clark, et al., University of Texas at Austin, Austin, USA, unpubl. res.

Fig. 2.

Gene expression overlap between Arabidopsis seeds and pollen and Ceratopteris spores. Numbers in the centre of the circles indicate the number of tissue-specific genes used for expression comparisons. The numbers in the overlapping shaded regions indicate the number of genes in common between the overlapping sets. Several representative genes are indicated from each comparison. Adapted from Salmi et al. (2005) with permission from the American Society of Plant Biologists.

Fig. 3.

Representation of common elements involved in tip growth between spores and pollen tubes. The bottom half of the figure is devoted to participants in calcium movement, the tip region to membrane- and actin-associated elements, and the top half to enzymes and other signalling molecules. Solid boxes are used for proteins and membranes, dashed boxes for signalling molecules. The colour of the shapes indicates general activities: blue for membrane transporters; green for membrane-associated; red for enzymatic activities; yellow for membrane-bound compartments. Generic ‘effector’ boxes are used as placeholders for elements that are not yet known to be present or function in both spores and pollen. Thin arrows indicate interactions or products being made, thick arrows are used to indicate Ca²⁺ ion movements and their directions. The thin green lines near the tip represent fine, dynamic F-actin. Annexins and Ca-channels are shown touching the fine F-actin to indicate their possible binding to or modulation by it.