Novelties of the flowering plant pollen tube underlie diversification of a key life history stage

Abstract

The origin and rapid diversification of flowering plants has puzzled evolutionary biologists, dating back to Charles Darwin. Since that time a number of key life history and morphological traits have been proposed as developmental correlates of the extraordinary diversity and ecological success of angiosperms. Here, I identify several innovations that were fundamental to the evolutionary lability of angiosperm reproduction, and hence to their diversification. In gymnosperms pollen reception must be near the egg largely because sperm swim or are transported by pollen tubes that grow at very slow rates (< approximately 20 microm/h). In contrast, pollen tube growth rates of taxa in ancient angiosperm lineages (Amborella, Nuphar, and Austrobaileya) range from approximately 80 to 600 microm/h. Comparative analyses point to accelerated pollen tube growth rate as a critical innovation that preceded the origin of the true closed carpel, long styles, multiseeded ovaries, and, in monocots and eudicots, much faster pollen tube growth rates. Ancient angiosperm pollen tubes all have callosic walls and callose plugs (in contrast, no gymnosperms have these features). The early association of the callose-walled growth pattern with accelerated pollen tube growth rate underlies a striking repeated pattern of faster and longer-distance pollen tube growth often within solid pathways in phylogenetically derived angiosperms. Pollen tube innovations are a key component of the spectacular diversification of carpel (flower and fruit) form and reproductive cycles in flowering plants.

Fig. 1.

Variation in fertilization timing among seed plants. Data represent the earliest time reported from pollination until a pollen tube enters the micropyle of the ovule. The proportion of angiosperms in each time category is represented in color (801 reports) and that of gymnosperms in black (109 studies) (hence, the bars in the graph sum to two, not one). Dark blue, light blue, and magenta represent monocots, eudicots, and all other angiosperms, respectively. h, hours; d, days; m, months. See SI Text, Fertilization Intervals of Seed Plants and Table S1.

Fig. 2.

Origins of rapid fertilization syndromes among major seed plant lineages. Fertilization intervals are mapped onto the “Gnepine” phylogenetic hypothesis (16) under the assumption that the seed plant ancestor had a long fertilization interval. The polarity of terminal taxa was determined from a much larger analysis by using data from Fig. 1 (SI Text, Methods for Phylogenetic Reconstruction of Fertilization Timing). Fertilization intervals are short (black), moderate (dark gray), long (light gray), or equivocal (hashed line). *, excluding Pinaceae.

Fig. 3.

Pollen tube growth patterns in basal grade angiosperms. (A) Amborella trichopoda pollen tubes grow between stigmatic hairs (sh), but only one or a few enter a narrow stylar canal (sc), grow to the ovarian cavity (oc) and around the downward facing single ovule (o). (B) Nuphar polysepala pollen tubes grow intercellularly below the stigmatic surface (data not shown) then enter a wide stylar canal that opens into a multiovulate ovarian cavity (cw, carpel wall). (C) Pollen tubes of Austrobaileya scandens grow into a massive stigmatic secretion, then enter individual carpels through a cleft (cl) between the two stigmatic lobes (sl; only one shown) and follow the open stylar canal to the ovarian cavity (composite image). (D–I) Callose plugs from Amborella (D and E), Nuphar (F and G), and Austrobaileya (H and I). All stained with aniline blue (A, double-stained with DAPI). (Scale bars: A, 100 μm; B, C, 500 μm; D–I, 10 μm.)

Fig. 4.

Pollen tube pathway lengths of early-divergent angiosperms. Black bars, minimum distance from stigma to nearest egg (in apical ovule) along pollen tube pathway; gray bars, additional minimum distance to furthest egg (in basal-most ovule). Lack of a gray bar indicates either one ovule/carpel or all ovules at same level. Dashed lines represent maximum pollen tube pathway lengths of gymnosperms, in which pollen typically germinates on the nucellus (3 mm) or rarely on other parts of ovule or cone (9 mm). Taxa and traits are listed in Table S3 in same order. Major clades: AM, Amborella; NY, Nymphaeales plus Hydatellaceae; AU, Austrobaileyales; MO, Monocots; CH, Chloranthaceae; EM, Eumagnoliids; and ED, Eudicots.

Fig. 5.

The relationship between the fertilization interval and pollen tube pathway length in seed plants (both axes log scale). Typical gymnosperms are restricted to the darkest shaded box (12, 14), except for extremes represented by green diamonds. Basal grade angiosperms (purple diamonds) fall above the hand-fitted gymnosperm constraint line, but are conservative relative to the majority of phylogenetically derived angiosperms (only extremes are shown, blue diamonds). For Agathis, Gnetum, and red oaks, a light shaded diamond includes only the total period of active pollen tube growth, whereas dark diamonds represent the total fertilization interval. Data and references are in Table S2.