Abstract
The Caryophyllales have the highest diversity in androecial patterns among flowering plants with stamen numbers ranging from 1 up to 4,000. Thanks to the recent progress in reconstructing the phylogeny of core Caryophyllales, questions of floral evolution, such as the origin and diversification of the androecium, can be readdressed. Caryophyllales are unique among core eudicots in sharing an androecial ring meristem or platform with centrifugal development of stamens and petals. Stamens are basically arranged in two whorls and evolution within the clade depends on the shift of either the antesepalous or the alternisepalous whorls to an upper position on the ring meristem and the reduction of the other. Four main developmental phenomena are responsible for the high diversity in androecial patterns: (1) the sterilisation of the outermost stamens through a division of common primordia; (2) the secondary addition of stamens by a centrifugal initiation of supernumerary stamens superimposed on a lower stamen number; (3) the pairwise displacement of alternisepalous stamens to the middle of the outer sepals and their potential fusion, or as part of a pluristaminate androecium; (4) the inversed sequence, reduction and loss of antesepalous stamens. Shifts in stamen numbers depend on pressures of the calyx and carpels and changes in the number of the latter. These patterns are expressed differently in the three main evolutionary lines of core Caryophyllales and are systematically relevant: (1) A basal grade of Caryophyllales, culminating with Caryophyllaceae, Amaranthaceae, Stegnosperma and Limeum, has the antesepalous stamens initiated in upper position on the ring meristem, and alternisepalous stamens are preferentially reduced. Among the antesepalous whorl there is a progressive loss of stamens following a sequence inversed to sepal initiation. Petaloid staminodes are formed by the radial division of outer stamens. (2) The raphide-clade and Molluginaceae are characterized by alternisepalous stamens in upper position on the ring meristem, with a trend to secondary stamen multiplication, and loss of antesepalous stamens. (3) The Portulacineae share the pattern of the raphide clade, but some taxa show shifts to an upper position on the ring meristem of either antesepalous or alternisepalous stamens, linked with secondary multiplications and reduction of either whorl. Different floral characters are plotted on a recent cladogram of Caryophyllales. The data show a consistent correlation between shifting carpel and stamen numbers independent of perianth evolution. Comparative data suggest that the basic androecium of Caryophyllales consists of two whorls of five stamens, linked with an absence of petals, and the evolution of the androecium is a combination of reductions and secondary multiplications of stamens with a highly predictive systematic value.
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Acknowledgments
I thank Patricia Dos Santos and Sam Brockington for earlier discussions and for providing data used in this review. I am also grateful to Kester Bull and Sam Brockington for critical comments on an earlier version of the manuscript. Frieda Christie’s technical assistance with the SEM is acknowledged. I also thank the two reviewers for their helpful comments.
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Appendices
Appendix 1: Selected characters plotted on the phylogeny of Caryophyllales
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1.
Perianth derivation (Fig. 4)
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uniseriate, sepal derived: 0
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biseriate, bract and sepal-derived: 1
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biseriate, sepal and stamen-derived: 2
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multiseriate, sepal and stamen-derived: 3
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multiseriate, bract and sepal-derived: 4
-
-
2.
Calyx morphology
-
calyx sepaloid: 0
-
calyx completely petaloid: 1
-
calyx only petaloid at margins: 2
-
calyx only petaloid on adaxial side: 3
-
-
3.
Number of stamen whorls, including secondary increase (Fig. 5)
-
androecium of three whorls including outer staminodial petaloids: 0
-
androecium of two whorls including alternisepalous staminodial petaloids: 1
-
androecium of single whorl antesepalous: 2
-
androecium of single whorl alternisepalous (including the obhaplostemonous Plumbaginaceae): 3
-
Red dots indicate the presence of a secondary increase in stamen number superimposed on one, respectively two whorls.
-
-
4.
Position of upper stamens on androecial ring meristem (Fig. 6)
-
alternisepalous: 0
-
antesepalous: 1
-
No clear distinction between alternisepalous and antesepalous stamens arising at same level: 2
-
no obvious ring meristem: 3
-
-
5.
Initiation of the antesepalous stamen whorl (Fig. 7)
-
complete with acropetal initiation: 0
-
complete with inversed initiation: 1
-
incomplete with inversed initiation: 2
-
incomplete with acropetal initiation: 3
-
-
6.
Presence of staminodes
-
as petaloids: 0
-
as stublike structures: 1
-
as part of complex androecium: 2
-
staminodes absent: 3
-
-
7.
polyandry (also as red dots in Fig. 5)
-
division of complex primordia: 0
-
ring primordium: 1
-
absent: 2
-
-
8.
Carpel number (Fig. 8)
-
five-four: 0
-
three: 1
-
two: 2
-
one: 3
-
more than five: 4
-
-
9.
Carpel position
-
Isomerous—antesepalous: 0
-
Isomerous—alternisepalous: 1
-
Oligomerous—median or with two carpels abaxially: 2
-
Oligomerous—transversal or with two carpels adaxially: 3
-
Polymerous—pluricarpellate: 4
-
Appendix 2
See Table 2.
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Ronse De Craene, L.P. Reevaluation of the perianth and androecium in Caryophyllales: implications for flower evolution. Plant Syst Evol 299, 1599–1636 (2013). https://doi.org/10.1007/s00606-013-0910-y
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DOI: https://doi.org/10.1007/s00606-013-0910-y