Size-dependent variation in plant form.

The study of organic form has a long and distinguished history going at least as far back as Aristotle's Historia Anima¯lium, wherein he identified five basic biological processes that define the forms of animals (metabolism, temperature regulation, information processing, embryo development, and inheritance). Unfortunately, all of Aristotle's writings about plant forms are lost. We know of them only indirectly from his student Theophrastus's companion books, collectively called Historia Plantarum, wherein plant forms are categorized into annual herbs, herbaceous perennials, shrubs, and trees. The study of plant forms did not truly begin until the romantic poet and naturalist Goethe proposed the concept of a hypothetical 'Plant Archetype', declared "Alles ist Blatt", and first coined the word morphologie, which inspired the French anatomist Cuvier (who established the field of comparative morphology), the English naturalist Darwin (who saw his theory of evolution reinforced by it), and the Scottish mathematician D'Arcy Thompson (who attempted to quantify it).

The evolution of hydrophobic cell wall biopolymers: from algae to angiosperms.

The transition from an aquatic ancestral condition to a terrestrial environment exposed the first land plants to the desiccating effects of air and potentially large fluctuations in temperature and light intensity. To be successful, this transition necessitated metabolic, physiological, and morphological modifications, among which one of the most important was the capacity to synthesize hydrophobic extracellular biopolymers such as those found in the cuticular membrane, suberin, lignin, and sporopollenin, which collectively reduce the loss of water, provide barriers to pathogens, protect against harmful levels of UV radiation, and rigidify targeted cell walls. Here, we review phylogenetic and molecular data from extant members of the green plant clade (Chlorobionta) and show that the capacity to synthesize the monomeric precursors of all four biopolymers is ancestral and extends in some cases to unicellular plants (e.g. Chlamydomonas). We also review evidence from extant algae, bryophytes, and early-divergent tracheophytes and show that gene duplication, subsequent neo-functionalization, and the co-option of fundamental and ancestral metabolic pathways contributed to the early evolutionary success of the land plants.

Did meiosis evolve before sex and the evolution of eukaryotic life cycles?

Biologists have long theorized about the evolution of life cycles, meiosis, and sexual reproduction. We revisit these topics and propose that the fundamental difference between life cycles is where and when multicellularity is expressed. We develop a scenario to explain the evolutionary transition from the life cycle of a unicellular organism to one in which multicellularity is expressed in either the haploid or diploid phase, or both. We propose further that meiosis might have evolved as a mechanism to correct for spontaneous whole-genome duplication (auto-polyploidy) and thus before the evolution of sexual reproduction sensu stricto (i.e. the formation of a diploid zygote via the fusion of haploid gametes) in the major eukaryotic clades. In addition, we propose, as others have, that sexual reproduction, which predominates in all eukaryotic clades, has many different advantages among which is that it produces variability among offspring and thus reduces sibling competition.

The evo-devo of multinucleate cells, tissues, and organisms, and an alternative route to multicellularity.

Multinucleate cells, tissues, or organisms occur in 60 families of land plants and in five otherwise diverse algal lineages (Rhodophyceae, Xanthophyceae, Chlorophyceae, Ulvophyceae, and Charophyceae). Inspection of a morphospace constructed out of eight developmental processes reveals a large number of possible variants of multinucleate cells and organisms that, with two exceptions, are represented by one or more plant species in one or more clades. Thus, most of these permutations of developmental processes exist in nature. Inspection of the morphospace also shows how the siphonous body plan (a multinucleate cell with the capacity for indeterminate growth in size) can theoretically serve as the direct progenitor of a multicellular organism by a process similar to segregative cell division observed in siphonocladean algae. Using molecular phylogenies of algal clades, different evolutionary scenarios are compared to see how the multicellular condition may have evolved from a multinucleate unicellular progenitor. We also show that the siphonous progenitor of a multicellular organism has previously passed through the alignment-of-fitness phase (in which genetic similarity among cells/nuclei minimizes internal genomic conflict) and the export-of-fitness phase (in which genetically similar cells/nuclei collaborate to achieve a reproductively integrated multicellular organism). All that is theoretically required is the evolutionary acquisition of the capacity to compartmentalize its cytoplasm.

Ontogenetic changes in the numbers of short- vs. long-shoots account for decreasing specific leaf area in Acer rubrum (Aceraceae) as trees increase in size.

Specific leaf area (SLA) is reported to decrease with increasing plant size among dicot tree species despite a strong positive correlation between SLA and relative growth rate. This diminishing returns in SLA may result from changes in the relative numbers of different shoot types bearing leaves with different SLAs as trees increase in overall size. This ontogenetic shift hypothesis was examined for 15 Acer rubrum trees differing in basal stem diameter (0.01 m ≤ D ≤ 0.62 m). Detailed analyses of the largest tree showed that short-shoots produced leaves with significantly smaller SLA than the leaves produced by long-shoots regardless of the location of shoots within the canopy. A combination of random effect and split-plot (main-effect) ANOVA models showed that >94% of the variance observed for SLA was attributable to shoot type rather than to the location of leaves in the canopy. Further, with increasing trunk diameter, the number of short-shoots increased rapidly relative to the number of long-shoots. Although the leaves of short-shoots gain disproportionately more surface area per unit mass investment compared to the leaves produced by long-shoots, our data show that ontogenetic shifts occurring at the shoot and whole plant level account for size-dependent decreases in total canopy SLA.

Predicting the allometry of leaf surface area and dry mass.

The manner in which increases in leaf surface area S scale with respect to increases in leaf dry mass M(t) within and across species has important implications to understanding the ability of plants to harvest sunlight, grow, and ultimately reproduce. Thus far, no mechanistic explanation has been advanced to explain why prior work shows that the scaling exponent governing the S to M(t) relationship is generally significantly less than one (i.e., S ∝ M(t)(α < 1.0)) such that increases in M(t) yield diminishing returns with respect to increases in S across most species. Here, we show analytically why this phenomenon occurs and present equations that predict trends observed in the numerical values of scaling exponents for the S vs. M(t) relationships observed across dicot tree species and two aquatic vascular plant species.

Genetic effects on the biomass partitioning and growth of Pisum and Lycopersicon.

We examined a series of eight pea genotypes differing in three naturally occurring allelic mutations, i.e., af (afila), st (stipules reduced), and tl (tendril-less) and three species, five cultivars, and one interspecific hybrid of tomato differing in SP (SELF-PRUNING) allele composition to determine whether different phenotypes ontogenetically express different biomass partitioning patterns compared to the isometric partitioning pattern and an interspecific 3/4 scaling "rule" governing annual growth with respect to body mass. The slopes and "elevations" (i.e., α and log ß, respectively) of log-log linear regression curves of bivariate plots of leaf, stem, and root dry mass and of annual growth vs. total body mass were used to assess pattern homogeneity. The annual growth of all pea and tomato phenotypes complied with the 3/4 growth rule. The biomass partitioning patterns of all tomato phenotypes were statistically indistinguishable from the isometric pattern as were those of the pea wild type and three single-mutant genotypes. However, significant departures from the isometric (and pea wild type) biomass allocation pattern were observed for three genotypes, all of which were homozygous for the af allele. These results open the door to explore the heritability and genetics underlying the allometry of biomass partitioning patterns and growth.

Evidence for "diminishing returns" from the scaling of stem diameter and specific leaf area.

Research indicates that increases in total leaf area (A(T)) may fail to keep pace with increases in total leaf mass (M(L)) across plants differing in size (e.g., as measured by stem diameter, D). This "diminishing returns" hypothesis predicts that the scaling exponent for A(T) vs. M(L) will be less than one and that the exponent for specific leaf mass (i.e., A(T) / M(L)) vs. D will be negative. These predictions were examined using data from 46 plants ranging between 0.125 cm ≤ D ≤ 0.485 m across 25 woody dicot species. Standardized major axis slopes were used to quantify scaling exponents and random effects models were used to quantify species and size effects on the numerical values of exponents. The exponents for A(T) vs. M(L) and A(T) / M(L) vs. D differed among species and different species groupings. In general, the exponent for A(T) vs. M(L) was less than one and the exponent for A(T) / M(L) vs. D was negative, as predicted. However, random effects models indicated that species effects overshadowed size effects, although size effects were statistically significant. The diminishing returns hypothesis therefore receives statistical support, i.e., although the numerical values of exponents are "species-dependent," they are less than unity, as predicted by theory.

"Diminishing returns" in the scaling of functional leaf traits across and within species groups.

More than 5,000 measurements from 1,943 plant species were used to explore the scaling relationships among the foliar surface area and the dry, water, and nitrogen/phosphorus mass of mature individual leaves. Although they differed statistically, the exponents for the relationships among these variables were numerically similar among six species groups (ferns, graminoids, forbs, shrubs, trees, and vines) and within 19 individual species. In general, at least one among the many scaling exponents was <1.0, such that increases in one or more features influencing foliar function (e.g., surface area or living leaf mass) failed to keep pace with increases in mature leaf size. Thus, a general set of scaling relationships exists that negatively affects increases in leaf size. We argue that this set reflects a fundamental property of all plants and helps to explain why annual growth fails to keep pace with increases in total body mass across species.

Biomass partitioning and leaf N,P - stoichiometry: comparisons between tree and herbaceous current-year shoots.

We compare the biomass partitioning patterns and the nitrogen/phosphorus (N,P) stoichiometry of the current-year shoots of tree and herbaceous species and ask whether they scale in the same ways. Our analyses indicate that few statistically significant differences exist between the shoot biomass partitioning patterns of the two functional species-groups. In contrast, statistically significant N,P - stoichiometric differences exist between the two functional groups. Across all species, dry leaf mass scales nearly as the square of basal stem diameter and isometrically with respect to dry stem mass. However, total leaf N scales as the 1.37-power and as the 1.09-power of total leaf P across herbaceous and tree shoots, respectively. Therefore, tree shoots can be viewed as populations of herbs elevated by their older, woody herbaceous cohorts. However, tree leaf stoichiometry cannot be modelled in terms of herbaceous N,P - leaf stoichiometry.

A comparison between the record height-to-stem diameter allometries of Pachycaulis and Leptocaulis species.

BACKGROUND AND AIMS: The interspecific allometry of maximum plant height (Hmax) with respect to maximum basal stem diameter (Dmax) has been studied for leptocaulis dicot and conifer tree species. In contrast, virtually nothing is known about the interspecific allometry of pachycaulis species. Here, the interspecific allometries for palms, cacti and cycads are reported and compared with those of leptocaulis dicot and conifer tree species to determine whether pachycauly limits Hmax with respect to Dmax. METHODS: Data for each of a total of 1461 pachycaulis and leptocaulis species were gathered from the primary literature. The scaling exponent and the allometric constant of logHmax vs. logDmax reduced major axis regression curves (and their respective 95 % confidence intervals) were used to compare the four species groups. The stem slenderness ratio (Hmax/Dmax = Rmax) for each species was also computed to compare interspecific trends in trunk shape. KEY RESULTS AND CONCLUSIONS: Each of the four species groups is allometrically unique, i.e. no single 'canonical' maximum plant height to stem diameter allometry exists across all four species groups. Although pachycaulis does not intrinsically limit height, height is nevertheless limited by the size range of basal stem diameter occupied by each species group. Pachycaulis species achieve heights comparable to some leptocaulis species by virtue of very high slenderness ratios attended by an absence or paucity of stem branching. The diversity observed for pachycaulis stem allometries is likely the result of the independent evolutionary origins of this growth habit and the different anatomical strategies used to stiffen stems.

N, P, and C stoichiometry of Eranthis hyemalis (Ranunculaceae) and the allometry of plant growth.

We report the nitrogen (N), phosphorus (P), and carbon (C) stoichiometry for each of the five organ-types (leaves, aerial stems, reproductive organs, roots, and tubers) of 17 actively growing Eranthis hyemalis plants differing in size (as measured in g C). We also report the N, P, and C stoichiometry of 20 winterized tubers, which are the only perennial organs of this species. Comparisons between whole-plant and winterized N/C and P/C levels indicate that N was resorbed from aerial organs and stored in tubers by the end of the growing season. Leaves were substantial reservoirs for N and P. With few exceptions, N scaled isometrically with respect to C for each organ-type, whereas P scaled as the 3/4 power of C. Thus, N is proportional to P(3/4), which is proportional to C regardless of organ-type. Additionally, annual growth rate G of shoots (leaves and aerial stems) scaled as the -3 power of leaf N/P quotients such that G was proportional to the 3/4 power of leaf P. We suggest that these scaling relationships (together with previously reported allometric trends across herbaceous species) show that growth is constrained by organ-specific N and P allocation patterns (presumably to proteins and ribosomes, respectively).

Biomechanics and anatomy of Lycopersicon esculentum fruit peels and enzyme-treated samples.

We report the biomechanics and anatomy of fruit wall peels (before and after cellulase/pectinase treatment) from two Lycopersicon esculentum cultivars (i.e., Inbred 10 and Sweet 100 cherry tomatoes). Samples were tested before and after enzyme treatment in uniaxial tension to determine their rate of creep, plastic and instantaneous elastic strains, breaking stress (strength), and work of fracture. The fruit peels of both cultivars exhibited pronounced viscoelastic and strain-hardening behavior, but differed significantly in their rheological behavior and magnitudes of material properties, e.g., Inbred 10 peels crept less rapidly and accumulated more plastic strains (but less rapidly), were stiffer and stronger, and had a larger work of fracture than Sweet 100 peels. The cuticular membrane (CM) also differed; e.g., Sweet 100 CM strain-softened at forces that caused Inbred 10 to strain-harden. The mechanical behavior of peels and their CM correlated with anatomical differences. The Inbred 10 CM develops in subepidermal cell layers, whereas the Sweet 100 CM is poorly developed below the epidermis. Based on these and other observations, we posit that strain-hardening involves the realignment of CM fibrillar elements and that this phenomenon is less pronounced for Sweet 100 because fewer cell walls contribute to its CM compared to Inbred 10.