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, 2012, pls010

The Evolution of Pollen Germination Timing in Flowering Plants: Austrobaileya Scandens (Austrobaileyaceae)

Affiliations

The Evolution of Pollen Germination Timing in Flowering Plants: Austrobaileya Scandens (Austrobaileyaceae)

Joseph H Williams. AoB Plants.

Abstract

Background and aims: The pollination to fertilization process (progamic phase) is thought to have become greatly abbreviated with the origin of flowering plants. In order to understand what developmental mechanisms enabled the speeding of fertilization, comparative data are needed from across the group, especially from early-divergent lineages. I studied the pollen germination process of Austrobaileya scandens, a perennial vine endemic to the Wet Tropics area of northeastern Queensland, Australia, and a member of the ancient angiosperm lineage, Austrobaileyales.

Methodology: I used in vivo and in vitro hand pollinations and timed collections to study development from late pollen maturation to just after germination. Then I compared the contribution of pollen germination timing to progamic phase duration in 131 angiosperm species (65 families).

Principal findings: Mature pollen of Austrobaileya was bicellular, starchless and moderately dehydrated-water content was 31.5 % by weight and volume increased by 57.9 % upon hydration. A callose layer in the inner intine appeared only after pollination. In vivo pollen germination followed a logarithmic curve, rising from 28 % at 1 hour after pollination (hap) to 97 % at 12 hap (R(2) = 0.98). Sufficient pollen germination to fertilize all ovules was predicted to have occurred within 62 min. Across angiosperms, pollen germination ranged from 1 min to >60 h long and required 8.3 ± 9.8 % of the total duration of the progamic phase.

Significance: Pollen of Austrobaileya has many plesiomorphic features that are thought to prolong germination. Yet its germination is quite fast for species with desiccation-tolerant pollen (range: <1 to 60 h). Austrobaileya and other early-divergent angiosperms have relatively rapid pollen germination and short progamic phases, comparable to those of many insect-pollinated monocots and eudicots. These results suggest that both the pollen germination and pollen tube growth periods were marked by acceleration of developmental processes early in angiosperm history.

Figures

Fig. 1
Fig. 1
The anther and stigma of A. scandens. (A) Fully dehiscent anther. Scale bar = 500 µm. (B) Germinated pollen with pollen tubes growing through stigmatic secretion to open stylar canal (asterisk) of a single carpel. Scale bar = 200 µm.
Fig. 2
Fig. 2
Pollen germination of A. scandens. (A) Two-celled pollen from female phase flower (closed anther) with IKI-stained granules in vegetative (tube) cell cytoplasm. (B) Pollen from open anther in immersion oil, showing dehydrated state at presentation (DIC). (C) In vitro hydrated pollen, just before germination (DIC). (D) Immature pollen (female phase of flower) with AB staining of extra-apertural endexine (en) and isolated endexine in aperture wall (asterisk). (E) Mature pollen from open anther (AB). Note AB stain in a thin layer of endexine which is thickened at the aperture edge, absent in its margins and present in the centre of the apertural wall (asterisk). Clumps of AB-stained material (of tapetal origin) are associated with the outer apertural wall. Note also the bulging of intine through aperture, probably caused by partial hydration of pollen during fixation. (F) Pollen from open anther showing intine stained by ruthenium red. (G) In vitro germinated pollen showing AB stain in inner pollen wall and its continuity with the emerging inner tube wall. Note that the tube tip (asterisk) in the background lacks AB staining. (H) Emergence of pollen tube has ruptured part of pollen wall and pushed aside aperture covering. Note strong AB staining of a presumably callose annulus (ca) at base of tube. (I, J) A ring of AB-stained material is prominent at the proximal pole of many mature and germinated pollen grains, marking the location of the generative cell wall (gw). Scale bars = 10 µm. (I) Callose wall of generative cell inside of intine. (J) Remnants of callose wall of generative cell. (K) In vivo germinated pollen (3 hap) with faintly stained tube nucleus (tn) in association with the generative cell near the young pollen tube tip (asterisk) (DAPI). Pollen from (G), (H), (J) and (K) was fixed and stained 2 h after innoculation on growth medium. (A), (D–F) and (I) are from methacrylate sections. a, aperture; aw, aperture wall; g, generative cell; gn, generative cell nucleus; i, intine; td, tapetal deposits; v, vegetative cell nucleus. Scale bars = 20 µm, except where noted.
Fig. 3
Fig. 3
Timing of initial weight loss from fresh Austrobaileya pollen. On the y-axis, 1.00 represents standardized initial weight of pollen just after removal from anthers.
Fig. 4
Fig. 4
In vivo pollen germination timing in Austrobaileya. Bars are standard errors. N =7, 13, 13, 13, 10 and 6 hand pollinations from 1–12 hap, respectively.
Fig. 5
Fig. 5
In vivo pollen germination timing in angiosperms. (A) Time reported for pollen germination to occur (range: 1 min to 60 h). (B) Time to pollen germination as a proportion of the total time from pollination to fertilization (progamic phase). In both graphs, classes on the x-axis represent the number of hours (≤h) reported for the minimum duration of the progamic phase. The number of genera in each class is shown at the top. Asterisks represent Austrobaileya. Bars are standard errors.

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