| HOME | HELP | FEEDBACK | SUBSCRIPTIONS | ARCHIVE | SEARCH | TABLE OF CONTENTS |
|
|
|
|||||||
|
|||||||||
Developmental Biology and Developmental Genetics |
3 Department of Plant Biology, Cornell University, Ithaca, New York 14853 USA 4 Department of Botany and Plant Sciences, University of California, Riverside, California 92521 USA
Received for publication 27 September 2007. Accepted for publication 23 January 2008.
ABSTRACT
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., 
and log β, 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.
Key Words: af (afila) • allometry • Fabaceae • Lycopersicon esculentum • Lycopersicon pennellii • Lycopersicon pimpinellifolium • leaf morphology • Pisum sativum • scaling relationships • Solanaceae
Shortly after J. S. Huxley's seminal 1924 publication in which he formalized the general allometric equation (i.e., 
, where Y2 and Y1 are interdependent variables, β is the allometric constant, and is the scaling exponent), scaling analysis was used to quantitatively explore plant growth and morphogenesis (e.g., Pearsall, 1927; Albaum, 1938
; Richards and Kavanagh, 1943; Schüepp, 1945). This approach has continued to provide important insights into a variety of ecological and evolutionary phenomena, ranging from intraspecific competition and reproductive strategies to size-dependent effects on forest productivity and self-thinning (e.g., Samson and Werk, 1986; Weller, 1987; Weiner and Fishman, 1994; Weiner and Thomas, 2001). However, it was not until the work of Sinnott (1958) that a genetic basis of scaling phenomena was demonstrated by means of a correlation between the numerical values of scaling exponents and the genetic composition of phenotypes. Specifically, Sinnott showed that the slopes of log-log linear plots of cucurbit fruit length vs. width numerically "segregate" in a Mendelian manner when the data from F2 generation plants were compared to their parental stocks (Sinnott, 1958). Despite this early demonstration of the "heritability" of the scaling exponent, the subsequent development of statistical models for mapping specific quantitative trait loci underling allometric patterns in animal systems (Long et al., 2006; Wu and Lin, 2006), and ample evidence that single-gene mutations can result in dramatic phenotypic differences (Hilu, 1983; Gottlieb, 1984), few studies have continued the tradition of exploring whether scaling relationships are correlated with the genetic composition of plants.
In light of this omission, the objectives of this paper are twofold: first, to determine the extent to which the biomass partitioning and growth allometries of different genotypes and species differ with those previously demonstrated for diverse species, and, second, to identify the genetic basis for allometric differences observed among partitioning patterns. Prior work based on comparisons across diverse species lacking secondary growth (or possessing a limited capacity for it) indicates that the biomass partitioning pattern for leaf, stem, and root dry biomass (i.e., ML, MS, and MR, respectively) across different species is governed by scaling exponents are statistically indistinguishable from one, i.e., 
, where the allometric "constants" β1 and β2 are free to numerically vary among taxa due to differences in the absolute mass of organ types, or within a taxon as a consequence of different growing conditions or genotypes (Niklas and Enquist, 2001, 2002; Niklas, 2003, Niklas, 2004). This isometric pattern is also reported to describe the interspecific partitioning patterns observed for the body parts that are functionally equivalent to leaf, stem, and root among a limited number of green and brown algal macrophytes as well as charophytes (Chara and Nitella) and the siphonous alga Caulerpa (Niklas, 2006). In turn, this isometric partitioning pattern is linked conceptually to a 3/4 scaling relationship between annual growth in total dry body mass (G) and total dry body mass per plant (MT), i.e., 
(Niklas, 1994b; Niklas and Enquist, 2001). Because these two scaling relationships extend beyond the Chlorobionta, they were adduced to reflect fundamental constraints on plant growth and thus examples of adaptive convergent evolution rather than phyletic legacies (Niklas and Enquist, 2001; Niklas, 2006).
Here, we use this isometric partitioning pattern as a null hypothesis with which to compare the partitioning and growth patterns of eight Pisum sativum L. genotypes differing in three naturally occurring mutations on separate chromosomes that alter leaf architecture (Blixt, 1972; Marx, 1977, 1986, 1987; Meicenheimer et al., 1983; DeMason and Chawla, 2004a, b; Villani and DeMason, 1997, 1999, 2000, 2001). Combinations of these mutations are embedded in otherwise isogenic lines that are homozygous recessive for Mendel's stem length gene LE (which encodes for a gibberellin 3-ß-hydroxylase that converts GA20 to the bioactive GA1 form; see Lester et al. [1997]) and are thus "dwarf" in appearance. These three naturally occurring mutants are the af (afila), st (stipules reduced), and tl (tendril-less) leaf mutants. The afaf phenotype bears branched tendrils where leaflets normally occur; plants with the stst genotype have markedly reduced stipules compared to those of the wild type; and plants with the tltl genotype produce leaflets where tendrils on the wild type normally occur (Fig. 1). We also report the growth and dry mass partitioning patterns of three tomato species differing in SP (SELF-PRUNING) gene composition [i.e., Lycopersicon esculentum (L.) Mill., L. pimpinellifolium (L.) Mill., and L. pennellii (Correll) D'Arcy], five commercially well-known cultivars of L. esculentum, and one interspecific hybrid.
|
; Villani and DeMason, 1999). TL reduces the number of pinna pairs produced, increases blade length, increases pinna length at all pinna positions, and reduces pinna branching (Villani and DeMason, 1999). The interactions between these two genes are additive, antagonistic, or epistatic (Marx, 1977, Marx, 1987; Villani and DeMason, 1999). Also, the genes control pinna form within the constraints of the blade regions (proximal vs. distal) (Lu et al., 1996). The strength of each gene's influence depends on pinna position and can be described as occurring in a gradient. AF has stronger effects on the petiole and proximal pinnae, whereas TL has stronger effects on the distal and terminal pinnae (DeMason and Villani, 2001).
IAA and GA have long been known to influence leaf initiation, morphogenesis, and expansion, and both hormones are known to be particularly important in the regulation of pea leaf morphogenesis (DeMason, 2005; DeMason and Chawla, 2004a, b; Bai and DeMason, 2006). Shoot tips cultured on IAA and GA inhibitors produce leaves with reduced size and complexity with leaflets in place of tendrils in distal positions (DeMason and Chawla 2004a, b). Also, the expression of IAA- and GA-regulated genes, such as PIN1, PsPK2, LE, and UNI, is altered in the af and tl mutants compared to the wild type (DeMason and Chawla, 2004a, b; Bai et al., 2005; Bai and DeMason, 2006). Collectively, these results indicate that the interactive regulation of IAA and GA alters the expression of genes controlling leaf morphogenesis, including AF and TL, and thus might profoundly alter the pattern of leaf vs. stem (or root) biomass allocation during ontogeny.
The tomato SP gene was selected because it is known to regulate the vegetative-to-reproductive switching of sympodial meristems, thereby affecting plant height and inflorescence architecture. Specifically, spsp genotypes are determinate in growth and appear dwarfed due to reductions in internodal length (Atherton and Harris, 1986; Pnueli et al., 1998; Kim et al., 2006; Quinet et al., 2006). These genetic differences aside, we selected Pisum and Lycopersicon for study also because they differ in possessing self-supporting stems. All eight pea phenotypes have a vine growth habit. In contrast, all the Lycopersicon phenotypes have mechanically self-supporting vegetative stems (unless loaded by large amounts of ripening fruits). This phenotypic distinction was explored because little is known about the biomass partitioning patterns of vines or lianas (see, however, Niklas, 1994a) and because species with a vine growth habit might prove to be exceptions to the allometry observed for species with self-supporting stems.
Finally, we adopted a conservative approach to accepting or rejecting whether the allometry of a particular genotype agrees with that of the 1/1 and 3/4 patterns. That is, the allometry of a particular genotype is not rejected as statistically compliant with these patterns unless the numerical values of its scaling exponents statistically significantly deviate from 1/1 or 3/4 based on their 95% confidence intervals. This conservative approach was not adopted to validate the 1/1 and 3/4 patterns (which are viewed by us as null hypotheses about average species behavior) but rather in an effort to focus sharp attention on those genotypes that are most likely to shed light on how genotypic makeup affects the numerical values of allometric parameters, such as scaling exponents.
MATERIALS AND METHODS
Plant materials and growing conditions
Seeds for the AFAF STST TLTL, AFAF STST tltl, AFAF stst TLTL, afaf STST TLTL, AFAF stst tltl, and afaf STST tltl pea genotypes were obtained from the U.S. Department of Agriculture (Pullman, WA). Seeds for the afaf stst TLTL and afaf stst tltl genotypes were produced from crosses by one of the authors (D. DeMason). Seeds for all but the afaf stst TLTL and afaf stst tltl genotypes were planted on 24 April 2007; those of the afaf stst TLTL and afaf stst tltl genotypes were planted on 27 May 2007. All plants were grown under greenhouse conditions in vermiculite (to facilitate the removal of roots), fertilized five days per week with dilute Peters (Jack's Professional) 21–5–20 plus magnesium sulfate, and grown under natural day-length conditions. Plants were grown in individual 1801 cell insert packs (measuring 5 cm depth x 9 cm width and breadth) inserted in a tray measuring 25 cm x 51 cm. Specimens were in close to one another but not allowed to intertwine or touch.
Seeds for L. esculentum cultivars ‘Fireball' (SP–), ‘Fireball' (spsp), and ‘VF Gardener' (SP–) were obtained from Dr. Henry Munger (Cornell University, Ithaca, NY); seeds for L. esculentum cultivar ‘New Yorker' (spsp) were provided by Dr. Richard Robinson (Geneva Experimental Station, Geneva, NY); seeds for L. esculentum cultivar ‘Husky Red' (SP–) and L. pimpinellifolium (SP–) were purchased from Totally Tomatoes (Randolph, WI); and seeds for L. pennellii (SP–) were obtained from Dr. Charles Rick (University of California, Davis). The F1 L. esculentum ‘New Yorker' x L. pennellii hybrid was produced by E. D. Cobb. All tomato plants were grown under greenhouse conditions in the soil-less medium "Cornell mix" to facilitate the harvesting of roots (Boodley and Sheldrake, 1982). Plants were fertilized once every week with Scotts Blossom Booster (10–30–20). Natural day-length conditions were increased to 16 hours using 400W high-pressure sodium tubes.
Harvesting and sample preparation
One to three healthy plants for each genotype were selected and harvested weekly, or, in the case of pea lines for which old seeds germinated poorly (e.g., afaf stst TLTL and afaf stst tltl genotypes), every two or three weeks. Roots were harvested by removing the planting medium under running tap water. Roots and hypocotyls were excised as a unit at the cotyledonary node with a razor blade; leaves (including stipules) were removed from stems to leave internodes intact as much as possible; each organ -type was weighed after drying at room temperature to constant mass. No distinction was made regarding the size or maturation of leaves or stem internodes, i.e., all leaves and internodes were harvested regardless of their size or appearance.
In the case of peas, cotyledons were also harvested, dried, and weighed because log-log regression of paired dry mass measurements revealed nonlinear log-log trends for seedlings with attached cotyledons. These nonlinear trends, which were most pronounced for the afaf STST tltl, afaf stst TLTL, and afaf stst tltl genotypes, were ascribed to the effects of the allocation of nutrients stored in cotyledons to seedling organ growth and development. In all cases, the data gathered from seedlings lacking cotyledons were statistically well described by log-log linear regression curves.
Statistical protocols
Annual growth in biomass (original units grams dry mass per plant per year); dry leaf, stem, and root dry mass (ML, MS, and MR, respectively; original units, g); and total dry body mass (MT = ML + MS + MR) were log10-transformed. Preliminary statistical analyses showed that each log-log bivariate regression was linear (after the removal of data from pea seedlings still in possession of turgid cotyledons; see previous paragraph). Annual growth in total dry mass per plant (G) was computed as the quotient of MT (at harvest time) and the time between germination and harvesting; time intervals in days were converted into years such that G has units of grams per year. Mass measurements in grams were subsequently transformed into units of kilograms to provide data with units comparable to those previously published for tree-sized plants (i.e., G has units of kilograms per plant per year and MT has units of kilograms; see Niklas and Enquist, 2001, 2002; Niklas, 2003, Niklas, 2004).
Standardized major axis (also called reduced major axis) regression protocols were used to determine the slope (the "scaling exponent", i.e., ) and the "elevation" (Y-intercept or "allometric constant"; i.e., log β) of log-log linear relationships (i.e., see Sokal and Rohlf, 1981; Niklas, 1994b). These parameters were computed using the formulas = OLS/r and 
, where OLS is the ordinary least squares (OLS) regression slope, r is the OLS correlation coefficient, and 
denotes the mean log-value of variable Y. The software package Standardized Major Axis Tests and Routines, denoted as (S)MATR (Falster et al., 2003; see also Warton and Weber, 2002), was used to determine whether the numerical values of differed among data sets (and, in the case of the isometric allometric pattern, from one). Heterogeneity among regression curve elevations was also evaluated to assess genetic effects. However, this parameter is free to vary numerically across and within species and therefore was not used as a criterion to evaluate deviations from isometric patterns (see Introduction). Heterogeneity was rejected in all cases if P > 0.05.
RESULTS
We report the allometry of all three vegetative organs (see Tables 1, 2). However, among vegetative organs, the data acquired for roots are the most suspect in terms of accuracy, because of possible unobserved root necrosis and biomass turnover and because of the practical difficulties of removing potting media from very fine roots. Therefore, the allometry of leaf vs. stem mass (i.e., ML vs. MS) was emphasized over that of leaf (or stem) vs. root biomass allocation in interpreting the results presented here.
|
|
|
|
= 0.95 (95% CIs = 0.90, 0.99; r2 = 0.994), which agrees with the isometric interspecific pattern. Within each of the remaining five genotypes, the 95% CIs for ML vs. MS scaling exponents included or approached one (Table 1). Although the 95% CIs of the exponent governing the ML vs. MR relationship for the wild type and two genotypes (i.e., AFAF STST TLTL, AFAF stst tltl, and afaf stst tltl) included or approached one, and, in the case of the MS vs. MR relationship, the scaling exponent for the wild type was approximately equal to one (Table 1), the wild type was the only genotype with a biomass partitioning pattern that did not deviate from the isometric interspecific pattern in any way. Therefore, tests for slope heterogeneity between the wild type and the remaining seven pea genotypes identified those genotypes with biomass partitioning patterns that deviated from both the wild type and the isometric interspecific patterns (Table 1). Importantly, however, the 1/1 isometric allometric pattern and its corresponding 95% confidence limits (rather than those of the pea wild type) were used as the "statistical standard" by which to judge which genotypes complied with the general isometric intraspecific trend.
Based on slope heterogeneity comparisons, three genotypes allocated disproportionately significantly more mass to leaves with increasing stem mass (i.e., afaf STST tltl, afaf stst TLTL, and afaf stst tltl); three genotypes allocated disproportionately slightly more mass to the construction of leaves than to roots (i.e., AFAF stst TLTL, afaf STST TLTL, and afaf STST tltl); and, finally, one genotype disproportionately allocated more mass to the construction of stems compared to roots (i.e., AFAF stst TLTL), whereas two genotypes allocated less mass to stem construction compared to root construction (i.e., afaf stst TLTL and afaf stst tltl). The scaling exponents governing the partitioning patterns of all afaf genotypes therefore differed from both the wild type and the isometric interspecific patterns. The only exception was the AFAF stst TLTL genotype, which nevertheless differed from the MS vs. MR wild type and the isometric interspecific patterns (Table 1). It is noteworthy that each genotype with a scaling exponent significantly greater than 1.0 also had an "elevated" regression curve, which indicates these phenotypes have more massive leaves throughout their ontogeny compared to the wild type. Perhaps counterintuitively, the leaves of the afaf STST TLTL genotype did not deviate from the wild type pattern despite having large leaves and stipules compared to stst tltl genotypes, indicating that pea leaves with large surface areas are not a priori large in terms of their dry mass.
Despite the aforementioned differences in biomass partitioning patterns, annual growth scaled as the 3/4 power of total body mass across all eight phenotypes (Fig. 3B), i.e., = 0.78 (95% CI = 0.70, 0.89; r2 = 0.960).
Tomato genotypes
The scaling exponents governing the biomass partitioning patterns across the majority of species, within each cultivars, and within the spSP interspecific hybrid were statistically indistinguishable from one another, and, with comparatively few exceptions, had 95% CIs that included or approached one (Table 2). The principal exceptions were the scaling exponents for the ML vs. MS log-log linear regression curves observed for L. pennellii and the F1 interspecific hybrid, which were significantly less than one (i.e., = 0.81and 0.85, respectively), which nevertheless did not differ significantly from the corresponding -values observed for L. pimpinellifolium and L. esculentum (Table 2; Fig. 4A). These results suggested that spsp alters leaf vs. stem biomass partitioning but has no observable effect on leaf vs. stem (or root) partitioning when embedded in the L. pennellii genetic background. Likewise, spsp had no observable effect on biomass partitioning patterns in the L. esculentum genetic backgrounds examined by us.
|
= 0.75 (95% CI = 0.73, 0.77; r2 = 0.993).
Interspecific biomass partitioning and growth allometries
Across all pea and tomato genetically different phenotypes, the scaling exponent for ML vs. MS was 0.89 (95% CIs = 0.86, 0.92; r2 = 0.988), which was deemed to be in reasonable numerical agreement with one (Fig. 5A). The exponents for ML vs. MR and MS vs. MR were 1.08 (95% CIs = 1.03, 1.13; r2 = 0.972) and 1.21 (95% CIs = 1.44, 1.28; r2 = 0.962), respectively, which deviated marginally from the 
1 hypothesis. Across all pea and tomato plants, the exponent for G vs. MT was 0.77 (95% CIs = 0.74, 0.79; r2 = 0.990; Fig. 5B), which agreed numerically with the 3/4 scaling hypothesis and was statistically indistinguishable from the scaling exponent previously reported for dicot and conifer tree species, although the allometric constant for the growth rates of peas and tomatoes was numerically larger than that for woody species (Fig. 5C).
|
Our analyses indicate that some pea genotypes have different biomass partitioning patterns from both the pea wild type and the isometric interspecific partitioning patterns, whereas none of the tomato species or their cultivars differing in the SP allele deviate from the isometric interspecific pattern. These two taxa, therefore, are discussed separately. Before doing so, however, it is noteworthy that the deviations from the isometric pattern reported here for some pea genotypes are not attributable to the vine growth habit of Pisum, because the leaf to stem allocation patterns of the wild type and four mutant lines are statistically indistinguishable from those reported for diverse species with self-supporting stems.
Pea mutants
Among eight different genotypes, comparisons among the scaling exponents governing the biomass partitioning patterns for leaf vs. stem and leaf vs. root show that the exponents for plants homozygous for af typically have numerically larger exponents than those observed for either the wild type or the interspecific isometric pattern, which are themselves statistically indistinguishable (see Table 1; Fig. 1F–H). These genotypes also have numerically elevated allometric constants compared to the wild type or among genotypes homozygous for only one of the other two recessive alleles. Plants homozygous for two or more of the three recessive alleles therefore allocate disproportionately more dry mass to the construction of their leaves compared to stems or roots (i.e., high -values for ML vs. MS or MR) or they have leaves that are substantially more massive (i.e., high log β-values for ML vs. MS or MR) than either wild type plants or each of the other four genotypes.
These results suggest gene interactions among the af, st, and tl alleles, which are located on separate chromosomes, and draw attention to the af allele, which figures prominently in the genotypes identified as statistical outliers. This conclusion resonates with the observation that "The numerous phenotypes resulting from combinations of two or more mutants reveal aspects of gene action that are not evident in single substitutions" (Marx, 1987, p. 314), which produce novel phenotypes. Our results also agree with the interactive effects of the af, tl, and tl alleles described previously (Villani and DeMason, 1999) and with the hypothesis that both IAA and GA function to increase leaf size and complexity (DeMason and Chawla, 2004a, b; DeMason, 2005; Bai and DeMason, 2006).
As noted, plants homozygous for tl have leaflets where tendrils occur on the wild type (the acacia phenotype; see Vilmorin and Bateson, 1912; see Fig. 1C); plants homozygous for af produce numerous multibranched tendrils where leaflets normally occur on the wild type (the afila phenotype; see Goldberg, 1965; see Fig. 1D); and plants homozygous only for st have a marked reduction in stipule size (Pellew and Sverdrup, 1923; see Fig. 1E). The gene products of AF, ST, and TL have not yet been identified. However, extensive research by DeMason and coworkers has shown that the AF and TL gene effects on foliar development operate in an antiparallel manner (for a recent review, see DeMason, 2006) and that IAA and/or GA or their downstream signals regulate AF and TL gene expression. For example, it is suggested that TL is up-regulated by auxin and/or GA in basipetal gradients within developing leaf primordia, whereas AF might be downregulated by one or the other hormone, thereby creating antiparallel expression (DeMason and Chawla, 2006).
Finally, it is noteworthy that despite obvious if not striking differences among phenotypes and dry mass partitioning patterns among the eight pea genotypes, our analyses show that annual growth in dry mass per individual scales as the 3/4 power of total body mass. This allometry thus appears to be "invariant" with respect to 3/4 scaling pattern reported using a large and diverse constellation of species, although it is clear that the allometric "constants" governing this relationship can and do vary significantly among genotypes and taxa (Niklas and Enquist, 2001; see Fig. 5C). This result is consistent with the observations of Pyke and Hedley (1983) who report comparatively small differences among shoot growth rates and net photosynthetic rates per unit dry mass for wild type, afaf/STST, and afaf/stst seedlings, although both rates decline in this genotype ranking order.
Tomato
Our inter- and intraspecific comparisons of tomato allometry focused on the possible effects of SP gene, which is part of a gene family (Carmel-Goren et al., 2003) involved in regulating the vegetative-reproductive switch along the tomato compound shoot. The spsp genotype manifests a determinate compound shoot wherein successive sympodial segments develop progressively fewer and shorter internodes until the entire shoot is terminated by two consecutive inflorescences (Atherton and Harris, 1986). In contrast, SP– genotypes produce shoots with an indeterminate number of sympodia composed of longer internodes (see Pnueli et al., 1998, fig. 1). Thus, we anticipated that spsp and SP– genotypes would differ in their leaf and stem biomass allocation patterns. Yet, across three species, five L. esculentum cultivars, and the L. esculentum x L. pennellii hybrid (differing in shoot architecture, overall size, and genetic composition), statistical comparisons fail to show quantitatively significant differences in the scaling exponents and the allometric constants governing dry mass allocation to leaves, stems, and roots (see Table 2). In addition, with two exceptions, all the genotypes examined have a biomass partitioning pattern that is indistinguishable from the isometric interspecific pattern, i.e., the ML vs. MS scaling exponents observed for L. pennellii and the interspecific hybrid are numerically significantly less than one, thereby deviating from the isometric pattern by allocating less dry mass to the construction of leaves compared to stems. Yet, even these two exceptions have growth rates that scale as the 3/4 power of total body mass in a manner that is indistinguishable from that of Pisum, the other tomato genotypes examined by us, and the isometric interspecific pattern.
Concluding remarks
A sharp distinction must be drawn between intra- and interspecific allometric trends (Weiner, 2004; Niklas, 2006). Individual species are expected to differ in how they allocate dry mass to the construction of leaves, stems, and roots if for no other reason than because the absolute size and morphology of their body parts can vary among even closely related taxa. This phenomenology is evident from the numerical differences among the elevations of log-log linear regression curves describing leaf, stem, and root biomass allocation patterns for different genotypes and taxa (see Tables 1, 2 and Fig. 5C). However, when individual plants lacking substantial quantities of secondary tissues are drawn from diverse species and examined allometrically, their interspecific biomass partitioning pattern manifests a comparatively narrow degree of variation that, on average, complies with that of an isometric pattern (Niklas and Enquist, 2002). Similar analyses also reveal that annual growth in total dry mass per individual scales, on average, as the 3/4 power of total body mass (Niklas and Enquist, 2001). The underlying mechanism(s) for these phenomena have been extensively and intensely sought after, but remain unknown or problematic even from a theoretical perspective. This condition is particularly true in terms of what is known about their heritability and genetic basis.
The data presented here may be useful in this regard because they demonstrate clear consequences of naturally occurring developmental mutants on biomass partitioning patterns that deviate from the "norm" whether defined on the basis of the pea wild type or the broad interspecific pattern, which are governed by isometric exponents and essentially identical statistically. This finding opens the door to more detailed analyses using genetics and allometric tools capable of revealing the heritability and genetic mechanisms underlying the isometric biomass partitioning pattern. Such exploration would benefit from the analyses of other pea genes that alter the leaf size and phenotype and that are also known to be regulated by IAA and GA, e.g., the phenotype of the uni (unifoliata) mutant has trifoliate to single leaf blades and wild type petioles and stipules and the phenotype of the milder mutant allele known as uni-tac (tendrilled acacia) whose leaves have a terminal leaflet and reduced numbers of tendril pairs (Marx, 1987; DeMason and Schmidt, 2001; DeMason and Chawla, 2004a; DeMason and Chawla, 2006). In turn, this agenda may reveal something about the genetic basis of the 3/4 scaling "rule," which appears to be exceedingly hard to "break"—or, if broken, perhaps goes unseen because of lethal consequences. Indeed, the pea genotypes identified in this report as possessing significantly different allometries from both the interspecific and the pea wild type pattern would probably not survive under natural conditions because they have poor vegetative growth and produce few viable seeds compared to the wild type. In the case of these genotypes, genetic manipulation appears to have produced allometric "outliers" that are at a disadvantage biologically.
FOOTNOTES
1 The authors thank Drs. M. Christianson (University of California, Berkeley), H.-C. Spatz (Freiburg University), and T. Cooke (University of Maryland), and one anonymous reviewer for providing constructive criticisms of an earlier version of this paper. Support from the College of Agriculture and Life Sciences, Cornell University is gratefully acknowledged. 
2 Author for correspondence (e-mail: kjn2{at}cornell.edu)
LITERATURE CITED
Albaum, H. G. 1938. Normal growth, regeneration and adventitious outgrowth formation in fern prothallia. American Journal of Botany 25: 37–44.[CrossRef][Web of Science]
Atherton, J. G., AND G. P. Harris. 1986. Flowering. In J. G. Atherton, and J. Rudich [eds.], The tomato crop, 167–200. Chapman and Hall, New York, New York, USA.
Bai, F., AND D. A. DeMason. 2006. Hormone interactions and regulation of Unifoliata, PsPK2, PsPIN1 and LE gene expression in pea (Pisum sativum) shoot tips. Plant &Cell Physiology 47: 935–948.
Bai, F., J. C. Watson, J. Walling, N. Weeden, A. A. Santner, AND D. A. DeMason. 2005. Molecular characterization and expression of PSPK2, a PINOID-like gene from pea (Pisum sativum). Plant Science 168: 1281–1291.
Blixt, S. 1972. Mutation genetics in Pisum. Agri Hortique Genetica 30: 1–293.[Web of Science]
Boodley, J. W., AND J. J. Sheldrake. 1982. Cornell peat-lite mixes for commercial plant growing. Information Bulletin no. 43 Cornell Cooperative Extension, Cornell University, Ithaca, New York, USA.
Carmel-Goren, L., Y. S. Liu, E. Lifschitz, AND D. Zamir. 2003. The SELF-PRUNING gene family in tomato. Plant Molecular Biology 52: 1215–1222.[CrossRef][Web of Science][Medline]
DeMason, D. A. 2005. Auxin-cytokinin and auxin-gibberellin interactions during morphogenesis of the compound leaves of pea (Pisum sativum). Planta 222: 151–166.[CrossRef][Web of Science][Medline]
DeMason, D. A. 2006. Auxin/gibberellin interactions in pea leaf morphogenesis. Botanical Journal of the Linnean Society 150: 45–59.[CrossRef][Web of Science]
DeMason, D. A., AND R. Chawla. 2004a. Roles of auxin morphogenesis of the compound leaves of pea (Pisum sativum). Planta 218: 435–448.[CrossRef][Web of Science][Medline]
DeMason, D. A., AND R. Chawla. 2004b. Roles of auxin and Uni in leaf morphogenesis of the afila genotype of pea (Pisum sativum). International Journal of Plant Sciences 165: 707–722.[CrossRef][Web of Science]
DeMason, D. A., AND R. Chawla. 2006. Auxin/gibberellin interactions in pea leaf morphogenesis. Botanical Journal of the Linnean Society 150: 45–59.[CrossRef][Web of Science]
DeMason, D. A., AND R. J. Schmidt. 2001. Roles of the Uni gene in shoot and leaf development of pea (Pisum sativum): Phenotypic characterization and leaf development in the uni and uni-tac mutants. International Journal of Plant Sciences 162: 1033–1051.[CrossRef][Web of Science]
DeMason, D. A., AND P. J. Villani 2001. Genetic control of leaf development in pea (Pisum sativum). International Journal of Plant Sciences 162: 493–511.[CrossRef][Web of Science]
Falster, D. S., D. I. Warton, AND I. J. Wright. 2003. (S)MATR: Standardised major axis tests and routines, version 1.0. Website http://www.bio.mq.edu.au/ecology/SMATR.
Goldberg, J. B. 1965. Afila, a new mutation in pea (Pisum sativum L.). Boletin Genético 1: 27–28.
Gottlieb, L. D. 1984. Genetics and morphological evolution in plants. American Naturalist 123: 681–709.[CrossRef][Web of Science]
Hilu, K. W. 1983. The role of singe-gene mutations in the evolution of flowering plants. Evolutionary Biology 16: 97–128.[Web of Science]
Huxley, J. S. 1924. Constant differential growth-ratios and their significance. Nature 114: 895.[CrossRef]
Kim, D. H., M. S. Han, H. W. Cho, Y. D. Jo, M. C. Cho, AND B. D. Kim. 2006. Molecular cloning of a pepper gene that is homologous to SELF-PRUNING. Molecules and Cells 22: 89–96.[Web of Science][Medline]
Lester, D. R., J. J. Ross, P. D. Davies, AND J. B. Reid. 1997. Mendel's stem length gene (Le) encodes a gibberellin 3 beta-hydroxylase. Plant Cell 9: 1435–1443.[Abstract]
Long, F., Y. Q. Chen, J. M. Cheverud, AND R. Wu. 2006. Genetic mapping of allometric scaling laws. Genetical Research 87: 207–216.[CrossRef][Web of Science][Medline]
Lu, B., P. J. Villani, J. C. Watson, D. A. Demason, AND T. J. Cooke. 1996. The control of pinna morphology in wild-type and mutant leaves of garden pea (Pisum sativum L.). International Journal of Plant Sciences 157: 659–673.[CrossRef][Web of Science]
Marx, G. A. 1977. A genetic syndrome affecting leaf development in Pisum. American Journal of Botany 64: 273–277.[CrossRef][Web of Science]
Marx, G. A. 1986. Tendrilled acacia (tac): an allele at the uni locus. Pisum Newsletter 18: 49–52.
Marx, G. A. 1987. A suite of mutants that modify pattern formation in pea leaves. Plant Molecular Biology Reporter 5: 311–335.[CrossRef]
Meicenheimer, R. D., F. J. Muehlbauer, J. L. Hindman, AND E. T. Gritton. 1983. Meristem characteristics of genetically modified pea (Pisum sativum) leaf primordia. Canadian Journal of Botany 61: 3430–3437.
Niklas, K. J. 1994a. Comparisons among biomass allocation and spatial distribution patterns for some vine, pteridophyte, and gymnosperm shoots. American Journal of Botany 81: 416–421.
Niklas, K. J. 1994b. Plant allometry: The scaling of form and process. University of Chicago Press, Chicago, Illinois, USA.
Niklas, K. J. 2003. Reexamination of a canonical model for plant organ biomass partitioning. American Journal of Botany 90: 250–254.
Niklas, K. J. 2004. Plant allometry: Is there a grand unifying theory? Biological Reviews of the Cambridge Philosophical Society 79: 871–889.[Medline]
Niklas, K. J. 2006. A phyletic perspective on the allometry of plant biomass-partitioning patterns and functionally equivalent organ-categories. New Phytologist 171: 27–40.[CrossRef][Web of Science][Medline]
Niklas, K. J., AND B. J. Enquist. 2001. Invariant scaling relationships for interspecific plant biomass production rates and body size. Proceedings of the National Academy of Sciences, USA 98: 2922–2927.
Niklas, K. J., AND B. J. Enquist. 2002. On the vegetative biomass partitioning of seed plant leaves, stems, and roots. American Naturalist 159: 482–497.[CrossRef][Web of Science][Medline]
Pellew, C., AND A. Sverdrup. 1923. New observations on the genetics of pea. Journal of Genetics 13: 125–131.[Web of Science]
Pnueli, L., L. Carmel-Goren, D. Hareven, T. Gutfinger, J. Alvarez, M. Ganai, D. Zamir, AND E. Lifschitz. 1998. The SELF-PRUNING gene of tomato regulates vegetative to reproductive switching of sympodial meristems and is the ortholog of CEN and TFL1. Development 125: 1979–1989.[Abstract]
Pyke, K. A., AND C. L. Hedley. 1983. Growth and photosynthesis of mutant pea seedlings. Annals of Botany 52: 719–724.
Quinet, M., V. Dielen, H. Batoko, M. Boutry, A. Havelange, AND J. M. Kinet. 2006. Genetic interactions in the control of flowering time and reproductive structure development in tomato (Solanum lycopersicum). New Phytologist 170: 701–710.[CrossRef][Web of Science][Medline]
Richards, O. W., AND A. J. Kavanagh. 1943. The analysis of the relative growth gradients and changing form of growing organisms, illustrated by the tobacco leaf. American Naturalist 77: 385–399.[CrossRef][Web of Science]
Samson, D. A., AND K. S. Werk. 1986. Size-dependent effects on the analysis of reproductive effort in plants. American Naturalist 127: 667–680.[CrossRef][Web of Science]
Schüepp, O. 1945. Allometrie und Metamorphose. Konstruktion eines Schemas eines einfachen Fiederblattes. Verhandlung Naturforschende Gesellschaft Basal 56: 261–271.
Sinnott, E. W. 1958. The genetic basis of organic form. Annals of the New York Academy of Sciences 71: 1223–1233.[CrossRef][Web of Science][Medline]
Sokal, R. R., AND F. J. Rohlf. 1981. Biometry, 2nd ed. W. H. Freeman, New York, New York, USA.
Villani, P. J., AND D. A. DeMason. 1997. Roles of the Af and Tl genes in pea leaf morphogenesis: Characterization of the double mutant (afaftltl). American Journal of Botany 84: 1323–1336.[Abstract]
Villani, P. J., AND D. A. DeMason. 1999. Roles of the Af and Tl genes in pea leaf morphogenesis: leaf morphology and pinna anatomy of the heterozygotes. Canadian Journal of Botany 77: 611–622.
Villani, P. J., AND D. A DeMason. 2000. Roles of the Af and Tl genes in pea leaf morphogenesis: Shoot ontogeny and leaf development in the heterozygotes. Annals of Botany 85: 123–135.
Vilmorin, P. De, AND W. Bateson. 1912. A case of gametic coupling in Pisum. Proceedings of the Royal Society of London, B, Biological Sciences 84: 9–11.
Warton, D. I., AND N. C. Weber. 2002. Common slope tests for bivariate errors-in-variables. Biometry Journal 44: 161–174.[CrossRef]
Weiner, J., AND I. Fishman. 1994. Competition and allometry in Kochia scoparia. Annals of Botany 73: 263–271.
Weiner, J., AND S. C. Thomas. 2001. The nature of tree growth and the "age-related decline in forest productivity." Oikos 94: 374–376.[CrossRef][Web of Science]
Weiner, J. 2004. Allocation, plasticity and allometry in plants. Perspectives in Plant Ecology, Evolution and Systematics 6: 207–215.[CrossRef][Web of Science]
Weller, D. E. 1987. The interspecific size-density relationship among crowded plant stands and its implication for the –3/2 power rule of self-thinning. American Naturalist 133: 20–41.[CrossRef]
Wu, R., AND M. Lin. 2006. Functional mapping—how to map and study the genetic architecture of dynamic complex traits. Nature Reviews. Genetics 7: 229–237.[CrossRef][Web of Science][Medline]
This article has been cited by other articles:
|
|
 |
|
  T. L. Koontz, A. Petroff, G. B. West, and J. H. Brown Scaling relations for a functionally two-dimensional plant: Chamaesyce setiloba (Euphorbiaceae) Am. J. Botany, May 1, 2009; 96(5): 877 - 884. [Abstract] [Full Text] [PDF]
|
|
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||
| HOME | HELP | FEEDBACK | SUBSCRIPTIONS | ARCHIVE | SEARCH | TABLE OF CONTENTS |
