PERSPECTIVES
mathematical mechanism whereby the giant component emerges in an evolving network is related to the mechanism whereby a spreading disease in such a network becomes an epidemic (3). Perhaps there are nonclassical, but still natural, models for the spread of a disease in a network for which epidemics emerge in unexpected ways.
It is important to note that the results presented by Achlioptas et al. are given by computer simulation rather than formal mathematical proof. So it may be the case (although it seems unlikely) that for larger values of n, some other kind of behavior becomes apparent. Indeed, whether or not this happens is a very intriguing mathematical issue. This
question will certainly draw considerable attention in the near future, and its solution (like the solution of any mathematical problem that appears to be beyond the reach of the current state of the art in mathematical technique) may lead to deeper insights into the evolution of randomized network formation models in general.
References and Notes
1. A. Barabasi, R. Albert, Science 286, 509 (1999).
2. D. Watts, S. Strogatz, Nature 393, 409 (1998).
3. R. Durrett, Random Graph Dynamics (Cambridge Univ. Press, Cambridge, 2007).
4. M. Keeling, K. EamesJ. R. S. Interface 2, 295 (2005).
5. D. Achlioptas et at, Science 323,1453 (2009).
6. N. Alon, ]. Spencer, The Probabilistic Method (Wiley, New York, 2008).
7. M. Dyer et al., Assoc. Comput. Mach. 38,1 (1991).
8. M. Mitzenmacher, E. Upfal, Probability and Computing: Randomized Algorithms and Probabilistic Analysis (Cambridge Univ. Press, Cambridge, 2005).
9. R. Motwani, P. Raghavan, Randomized Algorithms (Cambridge Univ. Press, Cambridge, 1995).
10. M. Mezard et al., Science 297, 812 (2002).
11. P. Erdos, A. Renyi, Publ. Math. Inst. Hung. Acad. So. 5, 17 (1960).
12. B. Bollobas, Random Graphs (Cambridge Univ. Press, Cambridge, 2001).
13. S. Janson et al., Random Graphs (Wiley, New York, 2000).
14. C. Borgs, ]. Chayes, R. van der Hofstad, G. Slade, ]. Spencer, Random Struct. Algorithms 27,137 (2005).
15. B. Bollobas, S. Janson, 0. Riordan, Random Struct. Algorithms 31, 3 (2007).
16. I acknowledge National Science Foundation grant DMS-0701183.
10.1126/science.ll71297
PLANT SCIENCE
Paternal Patterning Cue
Ueli Grossniklaus
More than 2000 years ago, Aristotle reflected on the contributions of mother and father to their offspring and proposed that the mother provided "matter" while the father provided "form" (i). The former is best illustrated by the development of enucleated sea urchin eggs into normal plu-teus larvae without any contribution from the zygotic genome (2). In plants, it was long thought that any parental effects on embryo-genesis were nonexistent. Over the past decade, however, several mutations that exert maternal effects on embryogenesis have been described in the model plant Arabidopsis thaliana (3). On page 1485 ofthis issue, Bayer et al. (4) describe the first paternal effect on plant embryogenesis, demonstrating that a
Institute of Plant Biology and Zurich-Basel Plant Science Center, University of Zurich, Zollikerstrasse 107, 8008 Zurich, Switzerland. E-mail: grossnik@botinst.uzh.ch
temporal cue provided by the sperm cell triggers the events leading to the first asymmetric division of the plant embryo.
Unlike in animals, where the products of meiosis (cell division that forms gametes) differentiate directly into haploid egg and sperm (harboring one set of chromosomes), plant spores divide to form multicellular gameto-phytes. The male gametophyte (pollen) harbors two sperm cells, which are delivered to the female gametophyte (embryo sac) that is embedded in the ovule, the precursor of the seed. In flowering plants (such as Arabidopsis), one sperm fuses with the egg cell to form the zygote, whereas the second fuses with the central cell and develops into the endosperm, a nutritive tissue supporting the growth of the embryo. After fertilization, the zygote elongates and divides asymmetrically to form a small apical cell, the precursor of the embryo proper, and a large basal cell, which
A signaling factor in sperm couples fertilization to the first plant patterning event.
develops into a filamentous structure called the suspensor (see the figure). Arabidopsis zygotes that inherit a paternal mutant short suspensor (ssp) allele fail to elongate and show defects in suspensor development. In extreme cases, the suspensor is completely lacking, implicating SSP in promoting suspensor fate (4).
Bayer et al. show that in Arabidopsis, the SSP gene encodes an interleukin-1 receptor-associated kinase/Pelle-like kinase. This enzyme activates a signaling pathway in the zygote that involves the MAP kinase kinase kinase YODA (YDA) and the MAP kinases MPK3 and MPK6. This cascade of activated kinases (the YDA pathway) promotes elongation of the zygote and suspensor development (5, 6). The SSP protein contains an amino-terminal motif for myristoylation/palmitoyl-ation (diacylation), a central kinase domain, and a carboxyl-terminal tetratricopeptide repeat.
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Although membrane association through the diacyl modification and the repeats are essential for SSP function, the kinase domain is dispensable. These findings strongly suggest that SSP acts at the plasma membrane, possibly by recruiting a YDA pathway activator.
Interestingly, the ssp mutation affects early embryogenesis only if it is paternally inherited. Though parent-of-origin effects were already known to mule breeders in Asia Minor more than 3000 years ago (7), genetic parent-oforigin effects were only recognized in the 1950s. In plants, which can be regenerated from single cells in culture through somatic embryogenesis, parental effects influencing embryogenesis were not thought to play a crucial role. In general, parent-of-origin effects can be mediated through nonnuclear, cytoplasmic contributions by the gametes or through the nonequivalent contribution of maternal and paternal alleles. The former is well illustrated by maternal effects in the fruit fly Drosophila melanogaster, where body axis determination depends on maternally stored cytoplasmic products (8). The latter, referred to as genomic imprinting, has only been described in mammals and seed plants. In Arabidopsis, both types of parent-of-origin effects likely exist. The first maternal effect gene identified in Arabidopsis turned out to be regulated by genomic imprinting (9). Furthermore, about half of the female gameto-phytic mutants isolated to date show defects in early seed development (3), and most of the paternally inherited genome is silent or active only at a low level during the first few embryonic divisions in maize and Arabidopsis (10, 11). Both findings suggest that there may be extensive maternal control over early embryogenesis that is mediated, in part, by cytoplasmi-cally stored products (12).
The mechanism by which SSP exerts its paternal effect may provide a means to subvert this maternal predominance. Bayer et al. show that mRNAs encoding SSP are only present in mature sperm cells, where they are apparently not translated into protein. By contrast, SSP protein is transiently detectable in the zygote and endosperm, suggesting that it is produced from paternally provided transcripts upon fusion of the egg and central cell with the sperm cells. Given the complex complement of transcripts present in plant sperm cells (13, 14), more paternal effect genes may be discovered. Whether this mechanism evolved as a consequence of a parental conflict, as has been proposed for the evolution of genomic imprinting (9), remains to be determined.
The known mutations in Arabidopsis that disrupt imprinted loci show normal early embryonic development, but affect cell proliferation of embryo and endosperm at later
stages and eventually lead to seed abortion. By contrast, spp mutants are viable and have no effect on endosperm development, but affect the very first, asymmetric division of the zygote. Thus, SSP transcripts delivered to the zygote by the sperm provide a molecular cue that links fertilization to the first zygotic division, which establishes apical-basal polarity of the embryo. This mechanism ensures that the activation of the YDA signaling pathway can only occur after fertilization and, thus, provides a temporal cue to initiate embryogenesis. Such a temporal cue would be of particular importance if most factors required for early development are already stored in the egg (12). This leaves the question, however, as to how embryonic activation is (de)regulated in apomictic plants, in which an egg develops into an embryo in the absence of fertilization (15). Is the YDA signaling pathway activated independently of SSP, or is SSP expressed from the maternal allele in the egg of apomictic plants? Future investigations will reveal how prominent
CIRCADIAN RHYTHMS
Linking the Loops
C. Robertson McClung
The evolution of life on a rotating planet has placed a premium on the temporal coordination of biological function with dramatic daily changes in environment. Thus, organisms from cyanobacteria to humans have evolved circadian clocks, endogenous oscillators with periods approximating the solar day, which provide temporal organization of many biological processes. The circadian clocks of different taxonomic groups comprise unrelated proteins, suggesting multiple evolutionary origins. Despite this phylogenetic diversity, there is a common logic to the molecular circuitry of these clocks—they are composed of feedback loops with positive and negative components (1). On page 1481 of this issue, Pruneda-Paz et al. (2) solve a major puzzle in our understanding of the plant clock and provide mechanistic insight into the positive arm of a core oscillatory loop first described nearly a decade ago (3).
Circadian clocks are composed of multiple interlocked feedback loops (1). Such corn-
Department of Biological Sciences, Dartmouth College, Hanover, NH 03755, USA. E-mail: c.robertson.mcclung@ dartmouth.edu
paternal cues are to stimulate embryonic development, which predominantly depends on maternally provided factors, at least in animals and likely also in plants. In other words, how instructive is the Aristotelean paternal "form" to the maternal "matter"?
References
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2. E. B. Harvey, Biol. Bull. 71, 101 (1936).
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5. W. Lukowitz et al., Cell 116, 109 (2004).
6. H. Wang, N. Ngwenyama, Y. Liu, J. C. Walker, S. Zhang,
Plant Cell 19, 63 (2007).
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8. C. Niisslein-Vollhard, Dev. Suppl. 1, 1 (1991).
9. U. Grossniklaus, in Annual Plant Reviews: Plant Epigenetics, P. Meyer, Ed. (Blackwell, Sheffield, UK, 2005), pp. 174-200.
10. D. Grimanelli et al., Plant Cell 17, 1061 (2005).
11. J.-P. Vielle-Calzada et al., Nature 404, 91 (2000).
12. C. Baroux et al., Cold Spring Harb. Symp. Quant. Biol. 10.1101/sqb.2008.73.053 (2009).
13. F. Borges et al., Plant Physiol. 148, 1168 (2008).
14. M. L. Engel et al., Plant J. 34, 697 (2005).
15. R. A. Bicknell, A. M. Koltunow, Plant Cell 16 (suppl.)
S228 (2004).
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plexity may increase clock stability and enhance the flexibility of response to multiple exogenous and endogenous time cues, thus integrating environmental signals with metabolic and physiologic information (4). The resonance of the internal periodicity imposed by the endogenous circadian clock with the environmental period imposed by Earth's rotation is important for fitness. For example, net photosynthesis falls dramatically when internal and external periods diverge (5). Recently, it was shown that altered clock function contributes to the increased growth, called "hybrid vigor," observed in hybrids and allopolyploids (6).
The clock of the plant Arabidopsis thaliana includes at least three interlocked loops (7-9). The initial identification of a putative core clock feedback loop in plants came with the establishment of reciprocal regulation between two Myb transcription factors—CIRCADIAN CLOCK ASSOCIATED 1 (CCA1) and LATE ELONGATED HYPOCOTYL (LHY)—and a pseudo-response regulator (PRR) called TIMING OF CAB EXPRESSION 1 (TOC1) (3). CCA1 and LHY also participate in a second
A new module in the plant circadian clock provides a long-missing link in the oscillator.
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