Stomatal vs. genome size in angiosperms: the somatic tail wagging the genomic dog?

Abstract

Background and aims: Genome size is a function, and the product, of cell volume. As such it is contingent on ecological circumstance. The nature of 'this ecological circumstance' is, however, hotly debated. Here, we investigate for angiosperms whether stomatal size may be this 'missing link': the primary determinant of genome size. Stomata are crucial for photosynthesis and their size affects functional efficiency.

Methods: Stomatal and leaf characteristics were measured for 1442 species from Argentina, Iran, Spain and the UK and, using PCA, some emergent ecological and taxonomic patterns identified. Subsequently, an assessment of the relationship between genome-size values obtained from the Plant DNA C-values database and measurements of stomatal size was carried out.

Key results: Stomatal size is an ecologically important attribute. It varies with life-history (woody species < herbaceous species < vernal geophytes) and contributes to ecologically and physiologically important axes of leaf specialization. Moreover, it is positively correlated with genome size across a wide range of major taxa.

Conclusions: Stomatal size predicts genome size within angiosperms. Correlation is not, however, proof of causality and here our interpretation is hampered by unexpected deficiencies in the scientific literature. Firstly, there are discrepancies between our own observations and established ideas about the ecological significance of stomatal size; very large stomata, theoretically facilitating photosynthesis in deep shade, were, in this study (and in other studies), primarily associated with vernal geophytes of unshaded habitats. Secondly, the lower size limit at which stomata can function efficiently, and the ecological circumstances under which these minute stomata might occur, have not been satisfactorally resolved. Thus, our hypothesis, that the optimization of stomatal size for functional efficiency is a major ecological determinant of genome size, remains unproven.

Fig. 1.

Stomatal length distribution within each of the four main study areas. (A) Argentina^a: log₁₀(stomatal guard-cell length, μm) ± s.d. 1·42 ± 0·13, n = 59; (B) Spain^ab: 1·43 ± 0·11, n = 284; (C) Iran^bc: 1·47 ± 0·11, n = 475; (D) England^c: 1·47 ± 0·13, n = 745. ANOVA F_3,1559 = 13·1, P < 0·001. Here and in the remaining figures and tables, groupings with the same suffix are not statistically significantly different at P < 0·05 in Tukey (post-hoc) tests.

Fig. 2.

Stomatal length distribution within different life-history classes: (A) woody polycarpic perennials^a [log₁₀(stomatal guard-cell length, μm) ±s.d. 1·41 ± 0·10, n = 205]; (B) monocarpic perennials^ab (1·45 ± 0·09, n = 89); (C) annuals^ab (1·45 ± 0·11, n = 451); (D) herbaceous polycarpic perennials^b (1·47 ± 0·11, n = 658); (E) vernal geophytes (1·68 ± 0·16, n = 46). ANOVA F_4,1444 = 58·6, P < 0·001.

Fig. 3.

PCA ordination of 1186 angiosperm species from Argentina, England, Iran and Spain, on the basis of six leaf traits. Labels display traits with the highest eigenvector scores on PCA axes 1, 2 and 3, with the label with the highest score presented nearest the axis. In (A) and (B), the distribution of species with large stomata (>40 µm) and those with small stomata (<20 µm) is shown, as indicated in (A), and in (C) and (D) the distribution of C₃, C₄, CAM and vernal geophyte species is shown as indicated in (C).

Fig. 4.

(A) Diploids tend to have smaller stomata than related polyploids. Each datum point is an intrageneric diploid–polyploid pair (monocots, excluding Poaceae; Poaceae; and eudicots, as indicated). Paired t = 5·1, n = 70, P < 0·001; r = 0·74, P < 0·001. Here, and in the remaining tables and figures, an ‘international’ average stomatal size value is used for more widely distributed species. (B) Stomatal length for diploid species differs between families. The box plots include the median (central line), the first and third quarters (box) and outliers. The 14 families illustrated (Amaranthaceae, Apiaceae, Asteraceae, Brassicaceae, Caprifoliaceae, Caryophyllaceae, Fabaceae, Lamiaceae, Orchidaceae, Plantaginaceae, Poaceae, Polygonaceae, Ranunculaceae and Rosaceae) are identified by their first three letters and phylogenetically ordered as recommended by Haston et al. (2007). ANOVA F_13,305 = 29·43, P < 0·001. Here ‘diploidy’ relates to the familial base chromosome number as given in Raven (1975) except for Orchidaceae, where, using Bateman et al. (2003), ploidy was assessed in relation to clade base number. Families with the same letters are not statistically significantly different at P < 0·05 in Tukey (post-hoc) tests. The mean value for stomatal size for all diploid species measured is identified by a broken line.

Fig. 5.

Examples of the relationship between stomatal and genome size. (A) All species: r² = 0·36, P < 0·001, n = 446. Eudicots (r² = 0·26, P < 0·001, n = 326); basal dicots (n = 3); monocots, excluding Poaceae (r² = 0·39, P < 0·001, n = 30); and Poaceae (r² = 0·53, P < 0·001, n = 87), as indicated. (B) Contrasted families: Ranunculaceae (r² = 0·64, P < 0·001, n = 23), and Fabaceae (r² = 0·64, P < 0·001, n = 46), as indicated. Other families: Asteraceae (r² = 0·08, P < 0·05, n = 51; minus Chrysanthemum segetum, r² = 0·08); Caryophyllaceae (r² = 0·23, P < 0·1, n = 15); Polygonaceae (r² = 0·32, P < 0·05, n = 13). (C) Contrasted tribes (Fabaceae): Fabeae (r² = 0·29, P < 0·01, n = 26); Trifolieae (r² = 0·67, P < 0·001, n = 13); and other (n = 7), as indicated. Tribes in other families: Asteraceae, Anthemideae (r² = 0·13, n.s., n = 17; minus Chrysanthemum segetum, r² = 0·30, P < 0·05, n = 16); Lactuceae (r² = 0·50, P < 0·001, n = 18); Poaceae, Agrostideae (r² = 0·49, P < 0·01, n = 13); Aveneae (r² = 0·72, P < 0·001, n = 11); Poeae (r² = 0·05, n.s., n = 19).