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Novelties of the flowering plant pollen tube underlie diversification of a key life history stage Joseph H. Williams* Department of Ecology and Evolution, University of Tennessee, Knoxville, TN 37996 Edited by Peter R. Crane, University of Chicago, Chicago, IL, and approved June 2, 2008 (received for review January 3, 2008) The origin and rapid diversification of flowering plants has puzzled angiosperm lineages. Thus, I performed hand pollinations and evolutionary biologists, dating back to Charles Darwin. Since that timed collections on representatives of three such lineages in the time a number of key life history and morphological traits have field [Amborella trichopoda, Nuphar polysepala, and Aus- been proposed as developmental correlates of the extraordinary trobaileya scandens; see supporting information (SI) Text, Meth- diversity and ecological success of angiosperms. Here, I identify ods for Pollination Studies]. several innovations that were fundamental to the evolutionary Each of these species has an extremely short fertilization lability of angiosperm reproduction, and hence to their diversifi- interval—pollen germinates in Ͻ2 h, a pollen tube grows to an cation. In gymnosperms pollen reception must be near the egg ovule in Ϸ18 h, and to an egg in 24 h (Table 1). The window for largely because sperm swim or are transported by pollen tubes that fertilization must be short because the egg cell is already present grow at very slow rates (< Ϸ20 ␮m/h). In contrast, pollen tube at the time of pollination (Table 1) and this is also the case for growth rates of taxa in ancient angiosperm lineages (Amborella, species within a much larger group of early-divergent lineages Nuphar, and Austrobaileya) range from Ϸ80 to 600 ␮m/h. Com- (Table S2 and references in ref. 11). Early-divergent angio- parative analyses point to accelerated pollen tube growth rate as sperms have far shorter fertilization intervals than any gymno- a critical innovation that preceded the origin of the true closed sperm (Fig. 1) (12) except for Gnetales: intervals are 6–8 days carpel, long styles, multiseeded ovaries, and, in monocots and in Gnetum (13) and 10–36 h in Ephedra (14, 15). eudicots, much faster pollen tube growth rates. Ancient angio- I used the data from Fig. 1 and Table 1 to map fertilization sperm pollen tubes all have callosic walls and callose plugs (in timing onto five major hypotheses of seed plant relationships contrast, no gymnosperms have these features). The early associ- (differing mainly in the placement of Gnetales) (16). I coded ation of the callose-walled growth pattern with accelerated pollen fertilization intervals as either ‘‘short’’ (i.e., Amborella/Ephedra tube growth rate underlies a striking repeated pattern of faster interval of Յ2 days), ‘‘moderate’’ (Illicium/Gnetum interval of and longer-distance pollen tube growth often within solid path- 2–7 days), or ‘‘long’’ (i.e., typical gymnosperm interval of Ͼ7 ways in phylogenetically derived angiosperms. Pollen tube inno- days). The common ancestor of extant seed plants was fixed as vations are a key component of the spectacular diversification of long (14). carpel (flower and fruit) form and reproductive cycles in flowering All five analyses infer that the common ancestor of extant plants. angiosperms (angiosperm CA) had a short fertilization interval, as summarized in Fig. 2 (see also SI Text, Methods for Phyloge- heterochrony ͉ key innovation ͉ modularity ͉ origin of angiosperms ͉ netic Reconstruction of Fertilization Timing, and Fig. S1). If evo-devo Gnetales is sister to pines, conifers, all other gymnosperms, or all other seed plants, two separate evolutionary transitions from lowering plants, or angiosperms, are thought to have origi- long to short fertilization intervals are inferred: one in the Fnated in an environment where rapid reproduction was common ancestor of Ephedra (or Gnetales) and one in the advantageous (1). Virtually all of their most defining features, angiosperm CA. However, if Gnetales is sister to angiosperms a including the flower, closed carpel, highly reduced male and single origin of the short fertilization interval in their common female gametophytes, double fertilization, sexually formed ancestor is supported. polyploid endosperm, and an exceptionally short pollination-to- fertilization interval (progamic phase), are thought to have Developmental Origins of Rapid Fertilization Syndromes in evolved under selection for a faster reproductive cycle (1–6). To Seed Plants understand what changes may have contributed to speeding the In seed plants, pollination (pollen reception by ovule or carpel) progamic phase, I undertook a series of comparative analyses of and fertilization (sperm fusion with egg cell) are key landmarks the interacting ontogenies that determine fertilization timing in for the development of the male gametophyte within sporophytic EVOLUTION seed plants. tissues. The plesiomorphic condition is that pollination occurs A survey of Ͼ900 studies, covering 130 seed plant families and near the beginning of megagametogenesis (14) and fertilization 717 taxa, indicates that the time interval between pollination and occurs after a long period of development of a large female fertilization (hereafter, ‘‘fertilization interval’’) ranges from 10 h gametophyte (13–15). Basal grade angiosperms retained the to Ͼ12 months in gymnosperms and from 15 min to Ͼ12 months plesiomorphic seed plant feature of pollination near the onset of in angiosperms (Fig. 1). Because angiosperms generally have megagametogenesis (refs. 4, 17, and Table 1). Because all much shorter fertilization intervals, it has long been supposed angiosperms have exceptionally small female gametophytes (17), that shortening of the fertilization process accompanied the origin of angiosperms (1–5). But two alternative hypotheses have also been proposed: the short fertilization interval may have Author contributions: J.H.W. designed research, performed research, analyzed data, and evolved earlier in history, before the origin of angiosperms (6), wrote the paper. or later, in one or more derived angiosperm lineages (7). Our The author declares no conflict of interest. understanding of early angiosperm relationships, based on re- This article is a PNAS Direct Submission. cent molecular phylogenetic analyses (8–10), provides the op- *E-mail: [email protected]. portunity to distinguish among these alternatives. This article contains supporting information online at www.pnas.org/cgi/content/full/ Rates, timing, and duration of the fertilization process have 0800036105/DCSupplemental. not yet been characterized in newly defined ‘‘basal grade’’ © 2008 by The National Academy of Sciences of the USA www.pnas.org͞cgi͞doi͞10.1073͞pnas.0800036105 PNAS ͉ August 12, 2008 ͉ vol. 105 ͉ no. 32 ͉ 11259–11263 Downloaded by guest on September 26, 2021 0.4 a ia Angiosperms e n a e Gymnosperms h s p ra a m y 0.3 y /B e a a il * a e ll /N a a rs s rs r m a e r b b i e d o e d u e r a m o m n h a g if e t c o h o tr u e t c k n h e a b p b s i m o 0.2 y in o p n in m u a u c ri ll C G C E G P A N C A Illi T A 0.1 Proportion of taxa Proportion of 0 7d 5d 5h 8h 6m 2m 1m 72h 14d 36h 21d 48h 24h 12h <2h 12m >12m Time between pollination and fertilization Origin of extant angiosperms Fig. 1. Variation in fertilization timing among seed plants. Data represent the earliest time reported from pollination until a pollen tube enters the Fig. 2. Origins of rapid fertilization syndromes among major seed plant micropyle of the ovule. The proportion of angiosperms in each time category lineages. Fertilization intervals are mapped onto the ‘‘Gnepine’’ phylogenetic is represented in color (801 reports) and that of gymnosperms in black (109 hypothesis (16) under the assumption that the seed plant ancestor had a long studies) (hence, the bars in the graph sum to two, not one). Dark blue, light fertilization interval. The polarity of terminal taxa was determined from a blue, and magenta represent monocots, eudicots, and all other angiosperms, much larger analysis by using data from Fig. 1 (SI Text, Methods for Phyloge- respectively. h, hours; d, days; m, months. See SI Text, Fertilization Intervals of netic Reconstruction of Fertilization Timing). Fertilization intervals are short Seed Plants and Table S1. (black), moderate (dark gray), long (light gray), or equivocal (hashed line). *, excluding Pinaceae. fertilization in the angiosperm CA is inferred to have become shifted earlier in time as a result of an abbreviation of female the pollen tube pathway and reducing pollen germination time, gametophyte ontogeny (1–4). In contrast, Ephedra retains the whereas slow pollen tube growth rate is conserved. Basal grade angiosperms all have faster pollen tube growth presumed plesiomorphic state of late fertilization timing (after Ϸ ␮ development of a large female gametophyte), but is specialized in rates than any gymnosperm, ranging from 80 to 600 m/h (Table 1), and comparable rates were calculated from other that pollination occurs long after onset of megagametogenesis (15). studies (Table S2). Thus, the angiosperm CA is inferred to have Thus, quite different heterochronic processes underlie changes in achieved its short fertilization interval by accelerating pollen relative onset and offset timing of the progamic phase: a short tube growth. Importantly, all early-divergent angiosperms have fertilization interval arose in Ephedra primarily by delay of polli- pollen tubes with callose (1,3-␤-glucan) secondary walls. Callose nation, and in the angiosperm CA, largely by earlier fertilization. plugs of the pollen tube are also present in Amborella, Nuphar, In virtually all gymnosperms, pollen hydration and germina- and Austrobaileya (Fig. 3). Rapid pollen tube growth and the tion takes two or more days and the active period of pollen tube callose wall and plugs are clearly conspicuous synapomorphies of growth (excluding dormant periods) takes five days or more (13, angiosperms, yet these traits have so far received little attention.

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