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PubMed2002

Functional identification of AtTPS03 as (E)-beta-ocimene synthase: a monoterpene synthase catalyzing jasmonate- and wound-induced volatile formation in Arabidopsis thaliana.

(E)-beta-Ocimene is one of the most commonly found monoterpenes of the volatile blends that are emitted from leaves in response to damage by herbivores or mechanical wounding. (E)-beta-Ocimene is also a component of many floral scents. Airborne (E)-beta-ocimene emitted from plants can serve as a chemical cue for the attraction of parasitoids or predators of plant herbivores and also as an attractant for pollinating insects. Furthermore, exposure of plants to (E)-beta-ocimene can activate defense gene expression. In this paper, we describe cDNA cloning and functional characterization of a gene encoding a highly specialized (E)-beta-ocimene synthase, AtTPS03, from Arabidopsis thaliana (L.) Heynh. AtTPS03 was identified as a member of the large AtTPS gene family of putative terpene synthases. A cDNA for AtTPS03 was expressed in Escherichia coli and the enzyme function identified in vitro. The A. thaliana (E)-beta-ocimene synthase produces almost exclusively (E)-beta-ocimene (94%) with minor amounts of the related acyclic monoterpenes (Z)-beta-ocimene (4%) and myrcene (2%). Transcripts for AtTPS03 were up-regulated in leaves of Arabidopsis in response to mechanical wounding and treatment with jasmonic acid, concurrent with induced emission of (E)-beta-ocimene. AtTPS03 provides an important gene for probing plant-insect and possibly plant-plant interactions mediated by terpenoid volatiles.

Acyclic Monoterpenes↗
PubMed2003

Lysine-containing proteins in maize endosperm: a major contribution from cytoskeleton-associated carbohydrate-metabolizing enzymes.

We measured fresh weight, dry weight, total protein, and the amounts of several individual proteins during endosperm development in three varieties of maize ( Zea mays L.): W64A wild-type (WT) and opaque-2 (o2), and sweet corn (SW). By 28 days after pollination (DAP), fresh weight was much higher in WT and SW than in o2, but o2 had a higher dry weight and thus a much lower water content. By 28 DAP, protein concentration [mg (g tissue(-1))] was highest in o2 and lowest in WT, while the protein content (microg seed(-1)) was lowest in o2. The storage proteins, alpha- and gamma-zeins, were low initially, but by 28 DAP they comprised over 50% of the total protein in WT and SW, but only about 30% in o2. In all varieties, the cytoskeleton proteins, actin, tubulin and eEF1alpha, sedimented with the protein bodies at 30 g to 27,000 g in tissue homogenized in cytoskeleton-stabilizing buffer. Other cytoskeleton-associated proteins increased during development, including UDP-glucose starch glucosyltransferase (UDP-GSGT, EC 2.4.1.11), sucrose synthase 1 (SuSy-1, EC 2.4.1.13) and fructose-1,6 bisphosphate aldolase (FBA, EC 4.1.2.13). At 28 DAP, these cytoskeleton-associated proteins combined make up 27% (WT), 23% (SW) and 33% (o2) of the total protein. These proteins are all rather high (5-11%) in lysine, and so they contribute about 75% (WT), 67% (o2), and 51% (SW) of the total endosperm lysine. We conclude that efforts to elevate the levels of these proteins could make a significant contribution to the nutritional value of corn.

Actins↗
PubMed2003

Arabidopsis mutants affected in the transcriptional control of allene oxide synthase, the enzyme catalyzing the entrance step in octadecanoid biosynthesis.

Allene oxide synthase (AOS) catalyzes the entrance reaction in the biosynthesis of the octadecanoids 12-oxophytodienoic acid (OPDA) and jasmonic acid (JA). The enzyme is feedback-regulated by JA and thus a target of the JA-signalling pathway. A fusion genetic approach was used to isolate mutants in this signalling pathway. Seeds from transgenic Arabidopsis thaliana plants expressing the Escherichia coli uidA gene encoding beta-glucuronidase (GUS) under the control of the AOS promoter were mutagenized with ethylmethane sulfonate and the progeny was screened for individuals exhibiting constitutive expression of uidA in the absence of an added octadecanoid. From 21,000 mutagenized plants, 8 lines showing constitutive AOS expression were obtained. The mutant lines were characterized further and fell into four classes, I to IV. All showed signs of growth inhibition encompassing both shoot and root systems, and accumulated higher than normal levels of OPDA. Mutants belonging to classes I and IV failed to set seeds due to defects in flower development which prevented self-pollination. One mutant, designated cas1, was characterized in more detail and showed, in addition to elevated levels of AOS mRNA, AOS polypeptide, OPDA, and JA, constitutive expression of JA-responsive genes ( VSP2, PDF1.2). The cas1 mutation is recessive and affects a single locus. Using cleaved amplified polymorphic sequences (CAPS) and simple sequence length polymorphisms (SSLP), the mutated gene was mapped to chromosome IV next to the SSLP marker CIW7.

Arabidopsis↗
PubMed2003

Gene expression at early stages of Brassica napus seed development as revealed by transcript profiling of seed-abundant cDNAs.

Approximately 5000 plaques derived from a Brassica napus L. (canola) seed-cDNA library representing 15 days after pollination (DAP) were differentially screened for highly expressed genes at the early stages of seed development. Analysis of 104 differentially expressed sequence tags revealed 54 unique genes, of which 33 had putative homologues described in Arabidopsis thaliana (L.) Heynh. or B. napus. These encoded diverse proteins, ranging from proteins of unknown function to metabolic enzymes and proteins associated with cell structure and development. Twenty-five genes were only expressed in seeds, and 11 of these started to express as early as 5 or 10 DAP. The majority of the seed-specific genes that are expressed at early stages of seed development encoded proteins with high similarity to hypothetical Arabidopsis proteins. Tissue-specificity determined by Northern analysis revealed that four seed-specific genes were expressed only in seed coats and another five in both embryos and seed coats. Analysis of transcript profiles of seed-abundant as well as seed-specific genes, and their expression patterns, implies that the B. napus seed is undergoing an active cell proliferation during 10-20 DAP, while establishing metabolic networks for subsequent seed maturation.

Arabidopsis↗
PubMed2004

Expression of proteinase inhibitor II proteins during floral development in Solanum americanum.

The heterologous expression of serine proteinase inhibitor II (PIN2) proteins confers insect resistance in transgenic plants, but little is known of their endogenous roles. We have cloned two cDNAs encoding Solanum americanum PIN2 proteins, SaPIN2a and SaPIN2b. SaPIN2a is highly expressed in stem, particularly in the phloem, suggesting it could possibly regulate proteolysis in the sieve elements. When SaPIN2a was expressed in transgenic lettuce, we observed an inhibition of endogenous trypsin- and chymotrypsin-like activities. Here, we demonstrate that both SaPIN2a and SaPIN2b are expressed in floral tissues that are destined to undergo developmental programmed cell death (PCD), suggesting possible endogenous roles in inhibiting trypsin- and chymotrypsin-like activities during flower development. Northern and western blot analyses revealed that SaPIN2a and SaPIN2b mRNAs and proteins show highest expression early in floral development. In situ hybridization analysis and immunolocalization on floral sections, localized SaPIN2a and SaPIN2b mRNAs and their proteins to tissues that would apparently undergo PCD: the ovules, the stylar transmitting tissue, the stigma and the vascular bundles. Detection of PCD in floral sections was achieved using terminal deoxynucleotidyltransferase-mediated dUTP nick end labeling (TUNEL) analysis. Examination of the mid-style before, and 1 day after, pollination revealed that high expression of SaPIN2a and SaPIN2b in the style was inversely correlated with PCD.

Apoptosis↗
PubMed2005

ZmLrk-1, a receptor-like kinase induced by fungal infection in germinating seeds.

We report here on the identification and characterization of ZmLrk-1, a member of the Lrk class of receptor-like kinases in Zea mays. This gene was found to be located at the bin21.40 region on the short arm of maize chromosome 8, closely linked to the previously reported pseudogene of the same class psiZmLrk (originally called Zm2Lrk). Transient expression experiments in onion epithelium cells, using a ZmLrk-1:GFP fusion protein, indicate that ZmLrk-1 is a membrane protein. ZmLrk-1 is ubiquitously expressed in the maize plant, including roots and aerial parts. In seeds, ZmLrk-1 transcripts can be detected by in situ hybridization exclusively at the basal endosperm transfer cell layer during the first stages of development. However, from 14 days after pollination its transcripts are preferentially detected at the upper half of the kernel, including both the aleurone and the starchy endosperm. ZmLrk-1 expression is not induced after treatment with salicylic acid, jasmonic acid or wounding, but it clearly increases after infection of germinating seeds with Fusarium oxysporum. This suggests that ZmLrk-1 could be involved in a sensing system to activate plant defence mechanisms against fungal attacks during endosperm development and seed germination.

Amino Acid Sequence↗
PubMed2007

The floral volatile, methyl benzoate, from snapdragon (Antirrhinum majus) triggers phytotoxic effects in Arabidopsis thaliana.

Previously it has been shown that the floral scent of snapdragon flowers consists of a relatively simple mixture of volatile organic compounds (VOCs). These compounds are thought to be involved in the attraction of pollinators; however, little is known about their effect on other organisms, such as neighboring plants. Here, we report that VOCs from snapdragon flowers inhibit Arabidopsis root growth. Out of the three major snapdragon floral volatiles, myrcene, (E)-beta-ocimene, and methyl benzoate (MB), MB was found to be primarily responsible for the inhibition of root growth. Ten micromoles MB reduced root length by 72.6%. We employed a microarray approach to identify the MB target genes in Arabidopsis that were responsible for the root growth inhibition phenotype in response to MB. These analyses showed that MB treatment affected 1.33% of global gene expression, including cytokinin, auxin and other plant-hormone-related genes, and genes related to seed germination processes in Arabidopsis. Accordingly, the root growth of cytokinin (cre1) and auxin (axr1) response mutants was less affected than that of the wild type by the volatile compound: roots of the treated mutants were reduced by 45.1 and 56.2%, respectively, relative to untreated control mutants.

Antirrhinum↗
PubMed2001

Microautoradiographic localisation of a glucosinolate precursor to specific cells in Brassica napus L. embryos indicates a separate transport pathway into myrosin cells.

The in-situ localisation of a desulpho-glucosinolate precursor has been studied by microautoradiography of cryo-sections from immature seeds and pods of the high-glucosinolate Brassica napus L. cv. Argentine collected 23 days after pollination. After feeding with the tritium-labelled glucosinolate precursor [4,5-3H](beta-D-glucopyranosyl)-4-pentenethiohydroxamic acid, embryo radicles, cotyledons and pod-wall were frozen in liquid nitrogen. Cryotome sections were freeze-dried and coated with nuclear emulsion autoradiographic film. A distinct pattern of radioactivity derived from the glucosinolate precursor was found in specific cells in both radicle and cotyledons. In contrast, the labelling in pod walls was not cell specific, but general at the inner side of the pod wall. The results show that the glucosinolate/desulphoglucosinolate was localised in specific cells, in a pattern resembling that of myrosin cells known to contain myrosinase (EC 3.2.3.1). In addition [4,5-3H](beta-D-glucopyranosyl)-4-pentenethiohydroxamic acid was fed to immature seeds and pods of B. napus and a quantitative incorporation into 2-hydroxy-3-butenylglucosinolate and 3-butenyl-glucosinolate was observed. When [4,5-3H](beta-D-glucopyranosyl)-4-pentenethiohydroxamic acid was fed to 4-day-old seedlings the label was taken up by all tissues. We propose a model in which glucosinolate/desulphoglucosinolates are transported to myrosin cells to participate in the myrosinase-glucosinolate multifunctional defence system.

Adaptation, Physiological↗
PubMed1997

Cell wall (1-->3)- and (1-->3, 1-->4)-beta-glucans during early grain development in rice (Oryza sativa L.).

Immunogold labeling was used to study the distribution of (1-->3)-beta-glucans and (1-->3, 1-->4)-beta-glucans in the rice grain during cellularization of the endosperm. At approximately 3-5 d after pollination the syncytial endosperm is converted into a cellular tissue by three developmentally distinct types of wall. The initial free-growing anticlinal walls, which compartmentalize the syncytium into open-ended alveoli, are formed in the absence of mitosis and phragmoplasts. This stage is followed by unidirectional (centripetal) growth of the anticlinal walls mediated by adventitious phragmoplasts that form between adjacent interphase nuclei. Finally, the periclinal walls that divide the alveoli are formed in association with centripetally expanding interzonal phragmoplasts following karyokinesis. The second and third types of wall are formed alternately until the endosperm is cellular throughout. All three types of wall that cellularize the endosperm contain (1-->3)-beta-glucans but not (1-->3, 1-->4)-beta-glucans, whereas cell walls in the surrounding maternal tissues contain considerable amounts of (1-->3, 1-->4)-beta-glucans with (1-->3)-beta-glucans present only around plasmodesmata. The callosic endosperm walls remain thin and cell plate-like throughout the cellularization process, appearing to exhibit a prolonged juvenile state.

Cell Wall↗
PubMed2001

Regeneration of transgenic loblolly pine (Pinus taeda L.) from zygotic embryos transformed with Agrobacterium tumefaciens.

Embryos of 24 open-pollinated families of loblolly pine (Pinus teade L.) were used as explants to conduct in vitro regeneration. Then, Agrobacterium tumefaciens strain GV3101 harboring the plasmid pPCV6NFHygGUSINT was used to transform mature zygotic embryos of seven families of loblolly pine. The frequency of transformation varied among families infected with A. tumefaciens. The highest frequency (100%) of transient beta-glucuronidase (GUS)-expressing embryos was obtained from family 11-1029 with over 300 blue spots per embryo. Expression of the GUS reporter gene was observed in cotyledons, hypocotyls, and radicles of co-cultivated mature zygotic embryos, as well as in callus and shoots derived from co-cultivated mature zygotic embryos. Ninety transgenic plants were regenerated from hygromycin-resistant callus derived from families W03. 8-1082 and 11-1029. and 19 transgenic plantlets were established in soil. The presence of the GUS gene in the plant genome was confirmed by polymerase chain reaction. Southern blot, and plant DNA/T-DNA junction analysis. These results suggest that an efficient A. tumefaciens-mediated transformation protocol for stable integration of foreign genes into loblolly pine has been developed and that this transformation system could be useful for future studies on transferring economically important genes to loblolly pine.

Agrobacterium tumefaciens↗
PubMed2002

Development of molecular markers for screening of Alnus nepalensis (D. Don) genotypes for the nitrogenase activity of actinorhizal root nodules.

Alnus nepalensis (D. Don), an alder species, is an actinorhizal tree found in the hilly regions of Eastern and Northeastern India. It is useful in the reclamation of wastelands generated by land slips, shifting agriculture and coal mining. To maximise the soil regeneration capacity of alder plantations, it would be useful to be able to select superior alder genotypes at the nursery level. Conventional methods of genotype screening are difficult to apply to open-pollinated forest trees. It would be beneficial if molecular markers could be developed for early screening. The study reported here was conducted to assess the feasibility of developing PCR-based AFLP and RFLP screening tools for the selection of superior genotypes of this valuable tree with respect to their ability to support efficient nitrogen-fixing root nodules. It was found that a multi-site strategy, including the chloroplast rrn operon and the nuclear rRNA genes, yielded promising results. A molecular marker for genotypes that support nodules with low nitrogenase activity was also identified.

Alnus↗
PubMed2005

Identification of a new class of pistil-specific proteins of Petunia inflata that is structurally similar to, but functionally distinct from, the self-incompatibility factor HT.

Pollen-pistil interactions are thought to involve a wide variety of intercellular recognition events controlled by diverse proteins and other molecules. One of the best characterized interactions is the S-RNase-based gametophytic self-incompatibility (GSI) system found in Solanaceae, Rosaceae and Scrophulariaceae. Although the S specificity of the pistil and the pollen in these families is determined by the S locus-encoded proteins S-RNase and SLF/SFB, respectively, these proteins alone are not sufficient for operation of the GSI reaction. Other factors are also required and are classified into three groups. To date, the only known factor is the pistil-expressed small asparagine-rich protein HT-B in three solanaceous genera Nicotiana, Lycopersicon and Solanum. HT-B is a Group 2 factor that is required for pollen rejection but do not affect S-RNase expression; factors in the other groups have not yet cloned. Here, we identified a new class of HT-like proteins in the style of Petunia inflata and named it HTL. Through alternative splicing, it was found that two isolated homologous HTL cDNAs, HTL-A and HTL-B, derived from a single gene. Like HT-B, HTL showed pistil-specific accumulation as well as significant sequence similarity to HT including conserved cystein residues at the C-terminal region and a signal peptide for extracellular localization. However, unlike HT-B, HTL lacked an asparagine-rich domain. Thus, it represents a new class of HT proteins. To determine whether HTL is involved in GSI function, RNA silencing constructs for HTL-A and HTL-B were introduced into self-incompatible P. inflata. Although several transgenic lines showed no detectable levels of both HTL-A and HTL-B transcripts, they retained normal GSI function and produced large fruits upon compatible pollination. This suggests that since silencing of the HTL gene alone is not sufficient to affect reproductive physiology, the gene is functionally distinct from the GSI factor HT-B.

Flowers↗
PubMed2007

Validation of in silico-predicted genic SNPs in white clover (Trifolium repens L.), an outbreeding allopolyploid species.

White clover (Trifolium repens L.) is an obligate outbreeding allotetraploid forage legume. Gene-associated SNPs provide the optimum genetic system for improvement of such crop species. An EST resource obtained from multiple cDNA libraries constructed from numerous genotypes of a single cultivar has been used for in silico SNP discovery and validation. A total of 58 from 236 selected sequence clusters (24.5%) were fully validated as containing polymorphic SNPs by genotypic analysis across the parents and progeny of several two-way pseudo-testcross mapping families. The clusters include genes belonging to a broad range of predicted functional categories. Polymorphic SNP-containing ESTs have also been used for comparative genomic analysis by comparison with whole genome data from model legume species, as well as Arabidopsis thaliana. A total of 29 (50%) of the 58 clusters detected putative ortholoci with known chromosomal locations in Medicago truncatula, which is closely related to white clover within the Trifolieae tribe of the Fabaceae. This analysis provides access to translational data from model species. The efficiency of in silico SNP discovery in white clover is limited by paralogous and homoeologous gene duplication effects, which are resolved unambiguously by the transmission test. This approach will also be applicable to other agronomically important cross-pollinating allopolyploid plant species.

Arabidopsis↗
PubMed2001

Sequence comparisons among dispersed members of the Brassica S multigene family in an S9 genome.

Self-incompatibility (SI) systems prevent self-pollination and promote outbreeding. In Brassica, the SI genes SLG (for S-locus glycoprotein) and SRK (for S-receptor kinase) are members of the S multigene family, which share the SLG-like domain (S domain), which encodes a putative receptor. We have cloned members of the S multigene family from the S9 haplotype of B. campestris (syn. rapa). In addition, eight distinct genomic regions harboring 10 SLG/SRK-like genes were characterized in the present study. Sequence analysis revealed two novel SRK-like genes, BcRK3 and BcRK6 (for B. campestris receptor kinases 3 and 6, respectively). Other genes that were characterized included SFR2 (for S gene family receptor 2), SLR2 (for S locus related gene 2), and a pseudogene. Based on phylogenetic analysis of the nucleotide sequences of the S domain regions, SLG and SRK appear to be distinct from other members of the S multigene family. Linkage analysis showed that most members of the S multigene family are dispersed in the Brassica genome, and that SLR1 (S locus related gene 1) is not linked to the SLR2 in B. campestris.

Blotting, Southern↗
PubMed1999

Homologs of animal eyes absent (eya) genes are found in higher plants.

Homologs of the eyes absent (eya) gene in animals function at multiple stages in the development of organs. Their functional roles in the genetic network that regulates eye development in Drosophila have recently been extensively analyzed. A rice homolog of eya was identified from a cDNA library made from embryo RNA. The corresponding gene (OSEya1) encodes a conserved ED1 domain and a short N-terminal peptide. The ED1 domain of OSEya1 shows 25% identity and 36% similarity to the product of Drosophila eya. Mammalian and squid eya homologs show about 35% similarity to OSEya1. Homologous sequences were also found in the alfalfa EST database (53% identity and 65% similarity to OSEya1) and in the Arabidopsis genome sequence (63% identity). Therefore, eya homologs are present in both monocots and dicots. Three regions in the ED1 domain are well conserved in animals and plants. Plant eya products deduced from the nucleotide sequences also have short N-terminal peptides. The OSEya1 gene is located between the wx gene and the telomere on the short arm of chromosome 6. OSEya1 is expressed in the embryo, shoot apex, and caryopsis in rice. Expression in the embryo increases during embryogenesis until 7 days after pollination, with preferential localization in leaf primordia and the shoot apical meristem. Expression in the influorescence was observed in floral meristems. The functions of OSEya1 in higher plants are discussed and compared with those of their animal homologs. OSEya1 might regulate the morphogenesis of lateral organs as a subunit of a transcription factor.

Amino Acid Sequence↗
PubMed2003

Effects of male sterility on reproductive traits in gynodioecious plants: a meta-analysis.

Female fecundity advantage in gynodioecious plants is required for the spread and maintenance of this reproductive system. However, not all reproductive characters show female advantage in all species. We used a meta-analysis to summarise differences between females and hermaphrodites reported from the literature for several reproductive traits. Further we tested three hypotheses, (1) that female plants of species with many ovules produce more seeds per fruit while those with few ovules produce heavier seeds, (2) that females are more pollen limited than hermaphrodites, and (3) that floral sexual size dimorphism is more pronounced in species with few ovules, either because female reproductive success is less limited by pollen availability in such species or because flowers with few ovules require a smaller floral structure to protect the carpels. Overall, females compared to hermaphrodites produced more but smaller flowers, had higher fruit set, higher total seed production, and produced heavier seeds that germinated better. Species with many versus few ovules differed in female advantage for flower size dimorphism, flower number, fruit set and total seed production. However seed size, seed set per fruit and seed germination differences between females and hermaphrodites did not differ significantly between species with few and many ovules. We also found no evidence for differential pollen limitation between females and hermaphrodites. Degree of floral sexual size dimorphism differed significantly between species with few and many ovules. Though pistillate flowers were generally smaller than those of hermaphrodites, species with many ovules showed less difference in flower size between the sexes, suggesting either that the protective role of the perianth constrains the evolution of sexual size dimorphism in species with many ovules or that selection for adequate pollination in species with many ovules impedes the reduction in flower size of females.

Adaptation, Physiological↗
PubMed2003

Gender-specific floral and physiological traits: implications for the maintenance of females in gynodioecious Lobelia siphilitica.

A common gender dimorphism in angiosperms is gynodioecy, in which hermaphrodites and females co-occur. Females are at an inherent disadvantage because they can transmit their genes only through ovule production. One mechanism by which females can compensate for the loss of male function is by producing more seeds than hermaphrodites. As such, females should: (1) increase resource uptake to support higher seed production; and (2) allocate resources saved by the loss of male function to seed production. To test this hypothesis, we measured physiological and floral traits of gynodioecious Lobelia siphilitica, controlling for both environmental and genetic variation through a comparison of greenhouse-grown siblings. Pre-reproductive females had 14% higher area-based (Z=2.14; P=0.04) and 32% higher mass-based (Z=1.96; P=0.05) photosynthetic rate than hermaphrodites, suggesting that they have increased carbon acquisition by altering photosynthetic physiology. Female L. siphilitica produced flowers with 4-8% smaller corollas than hermaphrodites (all P<0.05), suggesting that females allocate resources away from floral structures used for pollinator attraction. The genetic correlation between genders for four floral and four physiological traits was significantly less than one but greater than zero, indicating that the evolution of gender dimorphism in response to sex-differential selection will be constrained. The allocation of resources saved by the loss of male function has been viewed as the most important mechanism allowing females of gynodioecious species to support higher seed production. Our data suggest that increased resource acquisition by females at pre-reproductive stages can also contribute to the maintenance of gender dimorphism in gynodioecious species.

Analysis of Variance↗
PubMed2003

Floral density, pollen limitation, and reproductive success in Trillium grandiflorum.

Decreases in floral density can disrupt mutualistic interactions between plants and their pollinators, and decrease reproductive success. I addressed the relationship between floral density and plant reproductive success using two experimental approaches: a pollen supplementation experiment in 12 populations of Trillium grandiflorum that naturally varied in floral density, and a transplant experiment in which floral density was manipulated in plots at four experimental sites. In the pollen supplementation experiments, the degree of pollen limitation, in terms of fruit set and seed set, decreased with floral density. Further, in the experimental sites, plant reproductive success increased asymptotically with floral density. These results demonstrate the value of simultaneously conducting experiments in both experimental sites and natural populations to understand how population density influences plant reproductive success. Factors that reduce the density of this perennial herb, such as habitat fragmentation and herbivory by white-tailed deer ( Odocoileus virginianus), should be expected to limit its reproduction.

Flowers↗