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1.
Circ Cardiovasc Qual Outcomes ; 16(5): e009652, 2023 05.
Article in English | MEDLINE | ID: mdl-37017087

ABSTRACT

BACKGROUND: The COVID-19 pandemic has evolved through multiple phases characterized by new viral variants, vaccine development, and changes in therapies. It is unknown whether rates of cardiovascular disease (CVD) risk factor profiles and complications have changed over time. METHODS: We analyzed the American Heart Association COVID-19 CVD registry, a national multicenter registry of hospitalized adults with active COVID-19 infection. The time period from April 2020 to December 2021 was divided into 3-month epochs, with March 2020 analyzed separately as a potential outlier. Participating centers varied over the study period. Trends in all-cause in-hospital mortality, CVD risk factors, and in-hospital CVD outcomes, including a composite primary outcome of cardiovascular death, cardiogenic shock, new heart failure, stroke, and myocardial infarction, were evaluated across time epochs. Risk-adjusted analyses were performed using generalized linear mixed-effects models. RESULTS: A total of 46 007 patient admissions from 134 hospitals were included (mean patient age 61.8 years, 53% male, 22% Black race). Patients admitted later in the pandemic were younger, more likely obese, and less likely to have existing CVD (Ptrend ≤0.001 for each). The incidence of the primary outcome increased from 7.0% in March 2020 to 9.8% in October to December 2021 (risk-adjusted Ptrend=0.006). This was driven by an increase in the diagnosis of myocardial infarction and stroke (Ptrend<0.0001 for each). The overall rate of in-hospital mortality was 14.2%, which declined over time (20.8% in March 2020 versus 10.8% in the last epoch; adjusted Ptrend<0.0001). When the analysis was restricted to July 2020 to December 2021, no temporal change in all-cause mortality was seen (adjusted Ptrend=0.63). CONCLUSIONS: Despite a shifting risk factor profile toward a younger population with lower rates of established CVD, the incidence of diagnosed cardiovascular complications of COVID increased from the onset of the pandemic through December 2021. All-cause mortality decreased during the initial months of the pandemic and thereafter remained consistently high through December 2021.


Subject(s)
COVID-19 , Cardiovascular Diseases , Myocardial Infarction , Stroke , Adult , United States/epidemiology , Humans , Male , Middle Aged , Female , Cardiovascular Diseases/diagnosis , Cardiovascular Diseases/epidemiology , Cardiovascular Diseases/therapy , Risk Factors , Pandemics , American Heart Association , COVID-19/diagnosis , COVID-19/therapy , COVID-19/epidemiology , Myocardial Infarction/diagnosis , Myocardial Infarction/epidemiology , Myocardial Infarction/therapy , Registries , Hospital Mortality , Stroke/diagnosis , Stroke/epidemiology , Stroke/therapy , Heart Disease Risk Factors
2.
Plant Reprod ; 34(4): 321-334, 2021 12.
Article in English | MEDLINE | ID: mdl-34302535

ABSTRACT

The vegetative cell of the angiosperm male gametophyte (pollen) functions as a free-living, single-celled organism that both produces and transports sperm to egg. Whole-genome duplication (WGD) should have strong effects on pollen because of the haploid to diploid transition and because of both genetic and epigenetic effects on cell-level phenotypes. To disentangle historical effects of WGD on pollen performance, studies can compare 1n pollen from diploids to neo-2n pollen from diploids and synthetic autotetraploids to older 2n pollen from established neo-autotetraploids. WGD doubles both gene number and bulk nuclear DNA mass, and a substantial proportion of diploid and autotetraploid heterozygosity can be transmitted to 2n pollen. Relative to 1n pollen, 2n pollen can exhibit heterosis due to higher gene dosage, higher heterozygosity and new allelic interactions. Doubled genome size also has consequences for gene regulation and expression as well as epigenetic effects on cell architecture. Pollen volume doubling is a universal effect of WGD, whereas an increase in aperture number is common among taxa with simultaneous microsporogenesis and pored apertures, mostly eudicots. WGD instantly affects numerous evolved compromises among mature pollen functional traits and these are rapidly shaped by highly diverse tissue interactions and pollen competitive environments in the early post-WGD generations. 2n pollen phenotypes generally incur higher performance costs, and the degree to which these are met or evolve by scaling up provisioning and metabolic vigor needs further study.


Subject(s)
Magnoliopsida , Polyploidy , Diploidy , Gene Duplication , Humans , Magnoliopsida/genetics , Pollen/genetics
4.
Circulation ; 143(24): 2332-2342, 2021 06 15.
Article in English | MEDLINE | ID: mdl-33200953

ABSTRACT

BACKGROUND: The coronavirus disease 2019 (COVID-19) pandemic has exposed longstanding racial and ethnic inequities in health risks and outcomes in the United States. We aimed to identify racial and ethnic differences in presentation and outcomes for patients hospitalized with COVID-19. METHODS: The American Heart Association COVID-19 Cardiovascular Disease Registry is a retrospective observational registry capturing consecutive patients hospitalized with COVID-19. We present data on the first 7868 patients by race/ethnicity treated at 88 hospitals across the United States between January 17, 2020, and July 22, 2020. The primary outcome was in-hospital mortality. Secondary outcomes included major adverse cardiovascular events (death, myocardial infarction, stroke, heart failure) and COVID-19 cardiorespiratory ordinal severity score (worst to best: death, cardiac arrest, mechanical ventilation with mechanical circulatory support, mechanical ventilation with vasopressors/inotrope support, mechanical ventilation without hemodynamic support, and hospitalization alone. Multivariable logistic regression analyses were performed to assess the relationship between race/ethnicity and each outcome adjusting for differences in sociodemographic, clinical, and presentation features, and accounting for clustering by hospital. RESULTS: Among 7868 patients hospitalized with COVID-19, 33.0% were Hispanic, 25.5% were non-Hispanic Black, 6.3% were Asian, and 35.2% were non-Hispanic White. Hispanic and Black patients were younger than non-Hispanic White and Asian patients and were more likely to be uninsured. Black patients had the highest prevalence of obesity, hypertension, and diabetes. Black patients also had the highest rates of mechanical ventilation (23.2%) and renal replacement therapy (6.6%) but the lowest rates of remdesivir use (6.1%). Overall mortality was 18.4% with 53% of all deaths occurring in Black and Hispanic patients. The adjusted odds ratios for mortality were 0.93 (95% CI, 0.76-1.14) for Black patients, 0.90 (95% CI, 0.73-1.11) for Hispanic patients, and 1.31 (95% CI, 0.96-1.80) for Asian patients compared with non-Hispanic White patients. The median odds ratio across hospitals was 1.99 (95% CI, 1.74-2.48). Results were similar for major adverse cardiovascular events. Asian patients had the highest COVID-19 cardiorespiratory severity at presentation (adjusted odds ratio, 1.48 [95% CI, 1.16-1.90]). CONCLUSIONS: Although in-hospital mortality and major adverse cardiovascular events did not differ by race/ethnicity after adjustment, Black and Hispanic patients bore a greater burden of mortality and morbidity because of their disproportionate representation among COVID-19 hospitalizations.


Subject(s)
COVID-19/pathology , Health Status Disparities , Hospitalization/statistics & numerical data , Aged , Aged, 80 and over , American Heart Association , COVID-19/ethnology , COVID-19/mortality , COVID-19/virology , Cardiovascular Diseases/complications , Cardiovascular Diseases/pathology , Comorbidity , Female , Hospital Mortality/ethnology , Humans , Logistic Models , Male , Middle Aged , Race Factors , Registries , Retrospective Studies , SARS-CoV-2/isolation & purification , Severity of Illness Index , United States
5.
Circ Cardiovasc Qual Outcomes ; 13(8): e006967, 2020 08.
Article in English | MEDLINE | ID: mdl-32546000

ABSTRACT

BACKGROUND: In response to the public health emergency created by the coronavirus disease 2019 (COVID-19) pandemic, American Heart Association volunteers and staff aimed to rapidly develop and launch a resource for the medical and research community to expedite scientific advancement through shared learning, quality improvement, and research. In <4 weeks after it was first announced on April 3, 2020, AHA's COVID-19 CVD Registry powered by Get With The Guidelines received its first clinical records. METHODS AND RESULTS: Participating hospitals are enrolling consecutive hospitalized patients with active COVID-19 disease, regardless of CVD status. This hospital quality improvement program will allow participating hospitals and health systems to evaluate patient-level data including mortality rates, intensive care unit bed days, and ventilator days from individual review of electronic medical records of sequential adult patients with active COVID-19 infection. Participating sites can leverage these data for onsite, rapid quality improvement, and benchmarking versus other institutions. After 9 weeks, >130 sites have enrolled in the program and >4000 records have been abstracted in the national dataset. Additionally, the aggregate dataset will be a valuable data resource for the medical research community. CONCLUSIONS: The AHA COVID-19 CVD Registry will support greater understanding of the impact of COVID-19 on cardiovascular disease and will inform best practices for evaluation and management of patients with COVID-19.


Subject(s)
Betacoronavirus , Cardiovascular Diseases/therapy , Coronavirus Infections/complications , Emergency Service, Hospital/standards , Guideline Adherence , Pneumonia, Viral/complications , Quality Improvement , Registries , American Heart Association , COVID-19 , Cardiovascular Diseases/epidemiology , Coronavirus Infections/epidemiology , Pandemics , Pneumonia, Viral/epidemiology , Public Health , SARS-CoV-2 , United States/epidemiology
7.
Ann Bot ; 125(6): 925-935, 2020 05 13.
Article in English | MEDLINE | ID: mdl-31957784

ABSTRACT

BACKGROUND AND AIMS: Pollen tube growth rate (PTGR) is an important single-cell performance trait that may evolve rapidly under haploid selection. Angiosperms have experienced repeated cycles of polyploidy (whole genome duplication), and polyploidy has cell-level phenotypic consequences arising from increased bulk DNA amount and numbers of genes and their interactions. We sought to understand potential effects of polyploidy on several underlying determinants of PTGR - pollen tube dimensions and construction rates - by comparing diploid-polyploid near-relatives in Betula (Betulaceae) and Handroanthus (Bignoniaceae). METHODS: We performed intraspecific, outcrossed hand-pollinations on pairs of flowers. In one flower, PTGR was calculated from the longest pollen tube per time of tube elongation. In the other, styles were embedded in glycol methacrylate, serial-sectioned in transverse orientation, stained and viewed at 1000× to measure tube wall thicknesses (W) and circumferences (C). Volumetric growth rate (VGR) and wall production rate (WPR) were then calculated for each tube by multiplying cross-sectional tube area (πr2) or wall area (W × C), by the mean PTGR of each maternal replicate respectively. KEY RESULTS: In Betula and Handroanthus, the hexaploid species had significantly wider pollen tubes (13 and 25 %, respectively) and significantly higher WPRs (22 and 18 %, respectively) than their diploid congeners. PTGRs were not significantly different in both pairs, even though wider polyploid tubes were predicted to decrease PTGRs by 16 and 20 %, respectively. CONCLUSIONS: The larger tube sizes of polyploids imposed a substantial materials cost on PTGR, but polyploids also exhibited higher VGRs and WPRs, probably reflecting the evolution of increased metabolic activity. Recurrent cycles of polyploidy followed by genome reorganization may have been important for the evolution of fast PTGRs in angiosperms, involving a complex interplay between correlated changes in ploidy level, genome size, cell size and pollen tube energetics.


Subject(s)
Magnoliopsida , Pollen Tube , Cross-Sectional Studies , Diploidy , Humans , Polyploidy
8.
Am J Bot ; 106(7): 1011-1020, 2019 07.
Article in English | MEDLINE | ID: mdl-31294836

ABSTRACT

PREMISE: Male gametophytes of most seed plants deliver sperm to eggs via a pollen tube. Pollen tube growth rates (PTGRs) of angiosperms are exceptionally rapid, a pattern attributed to more effective haploid selection under stronger pollen competition. Paradoxically, whole genome duplication (WGD) has been common in angiosperms but rare in gymnosperms. Pollen tube polyploidy should initially accelerate PTGR because increased heterozygosity and gene dosage should increase metabolic rates. However, polyploidy should also independently increase tube cell size, causing more work which should decelerate growth. We asked how genome size changes have affected the evolution of seed plant PTGRs. METHODS: We assembled a phylogenetic tree of 451 species with known PTGRs. We then used comparative phylogenetic methods to detect effects of neo-polyploidy (within-genus origins), DNA content, and WGD history on PTGR, and correlated evolution of PTGR and DNA content. RESULTS: Gymnosperms had significantly higher DNA content and slower PTGR optima than angiosperms, and their PTGR and DNA content were negatively correlated. For angiosperms, 89% of model weight favored Ornstein-Uhlenbeck models with a faster PTGR optimum for neo-polyploids, whereas PTGR and DNA content were not correlated. For within-genus and intraspecific-cytotype pairs, PTGRs of neo-polyploids < paleo-polyploids. CONCLUSIONS: Genome size increases should negatively affect PTGR when genetic consequences of WGDs are minimized, as found in intra-specific autopolyploids (low heterosis) and gymnosperms (few WGDs). But in angiosperms, the higher PTGR optimum of neo-polyploids and non-negative PTGR-DNA content correlation suggest that recurrent WGDs have caused substantial PTGR evolution in a non-haploid state.


Subject(s)
Biological Evolution , Cycadopsida/physiology , Magnoliopsida/physiology , Pollen Tube/growth & development , Polyploidy , Genome Size , Genome, Plant , Phylogeny
9.
Curr Top Dev Biol ; 131: 299-336, 2019.
Article in English | MEDLINE | ID: mdl-30612621

ABSTRACT

With the origin of pollination in ancient seed plants, the male gametophyte ("pollen") began to evolve a new and unique life history stage, the progamic phase, a post-pollination period in which pollen sexual maturation occurs in interaction with sporophyte-derived tissues. Pollen performance traits mediate the timing of the fertilization process, often in competition with other pollen, via the speed of pollen germination, sperm development, and pollen tube growth. Studies of pollen development rarely address the issue of performance or its evolution, which involves linking variation in developmental rates to relative fitness within populations or to adaptations on a macroevolutionary scale. Modifications to the pollen tube pathway and changes in the intensity of pollen competition affect the direction and strength of selection on pollen performance. Hence, pollen developmental evolution is always contextual-it involves both the population biology of pollen reaching stigmas and the co-evolution of sporophytic traits, such as the pollen tube pathway and mating system. For most species, performance evolution generally reflects a wandering history of periods of directional selection and relaxed selection, channeled by developmental limitations, a pattern that favors the accumulation of diversity and redundancy in developmental mechanisms and the genetic machinery. Developmental biologists are focused on finding universal mechanisms that underlie pollen function, and these are largely mechanisms that have evolved through their effects on performance. Here, we suggest ways in which studies of pollen performance or function could progress by cross-fertilization between the "evo" and "devo" fields.


Subject(s)
Biological Evolution , Gametogenesis, Plant , Plant Physiological Phenomena , Plants , Pollen/cytology , Pollen/physiology
10.
Front Plant Sci ; 8: 900, 2017.
Article in English | MEDLINE | ID: mdl-28659934

ABSTRACT

The geometries and topologies of leaves, flowers, roots, shoots, and their arrangements have fascinated plant biologists and mathematicians alike. As such, plant morphology is inherently mathematical in that it describes plant form and architecture with geometrical and topological techniques. Gaining an understanding of how to modify plant morphology, through molecular biology and breeding, aided by a mathematical perspective, is critical to improving agriculture, and the monitoring of ecosystems is vital to modeling a future with fewer natural resources. In this white paper, we begin with an overview in quantifying the form of plants and mathematical models of patterning in plants. We then explore the fundamental challenges that remain unanswered concerning plant morphology, from the barriers preventing the prediction of phenotype from genotype to modeling the movement of leaves in air streams. We end with a discussion concerning the education of plant morphology synthesizing biological and mathematical approaches and ways to facilitate research advances through outreach, cross-disciplinary training, and open science. Unleashing the potential of geometric and topological approaches in the plant sciences promises to transform our understanding of both plants and mathematics.

11.
Biochem Biophys Res Commun ; 487(3): 509-516, 2017 06 03.
Article in English | MEDLINE | ID: mdl-28396152

ABSTRACT

The early evolution of angiosperms was marked by a number of innovations of the reproductive cycle including an accelerated fertilization process involving faster transport of sperm to the egg via a pollen tube. Fast pollen tube growth rates in angiosperms are accompanied by a hard shank-soft tip pollen tube morphology. A critical actor in that morphology is the wall-embedded enzyme pectin methylesterase (PME), which in type II PMEs is accompanied by a co-transcribed inhibitor, PMEI. PMEs convert the esterified pectic tip wall to a stiffer state in the subapical flank by pectin de-esterification. It is hypothesized that rapid and precise targeting of PME activity was gained with the origin of type II genes, which are derived and have only expanded since the origin of vascular plants. Pollen-active PMEs have yet to be reported in early-divergent angiosperms or gymnosperms. Gene expression studies in Nymphaea odorata found transcripts from four type II VGD1-like and 16 type I AtPPME1-like homologs that were more abundant in pollen and pollen tubes than in vegetative tissues. The near full-length coding sequence of one type II PME (NoPMEII-1) included at least one PMEI domain. The identification of possible VGD1 homologs in an early-diverging angiosperm suggests that the refined control of PMEs that mediate de-esterification of pectins near pollen tube tips is a conserved feature across angiosperms. The recruitment of type II PMEs into a pollen tube elongation role in angiosperms may represent a key evolutionary step in the development of faster growing pollen tubes.


Subject(s)
Carboxylic Ester Hydrolases/genetics , Magnoliopsida/genetics , Pollen Tube/genetics , Amino Acid Sequence , Carboxylic Ester Hydrolases/metabolism , Computational Biology , Magnoliopsida/enzymology , Phylogeny , Pollen Tube/enzymology , Pollen Tube/growth & development
12.
Am J Bot ; 103(3): 365-74, 2016 Mar.
Article in English | MEDLINE | ID: mdl-26980838

ABSTRACT

Ecologists and evolutionary biologists have been interested in the functional biology of pollen since the discovery in the 1800s that pollen grains encompass tiny plants (male gametophytes) that develop and produce sperm cells. After the discovery of double fertilization in flowering plants, botanists in the early 1900s were quick to explore the effects of temperature and maternal nutrients on pollen performance, while evolutionary biologists began studying the nature of haploid selection and pollen competition. A series of technical and theoretic developments have subsequently, but usually separately, expanded our knowledge of the nature of pollen performance and how it evolves. Today, there is a tremendous diversity of interests that touch on pollen performance, ranging from the ecological setting on the stigma, structural and physiological aspects of pollen germination and tube growth, the form of pollen competition and its role in sexual selection in plants, virus transmission, mating system evolution, and inbreeding depression. Given the explosion of technical knowledge of pollen cell biology, computer modeling, and new methods to deal with diversity in a phylogenetic context, we are now more than ever poised for a new era of research that includes complex functional traits that limit or enhance the evolution of these deceptively simple organisms.


Subject(s)
Biological Evolution , Ecological and Environmental Phenomena , Pollen/physiology , Haploidy , Inbreeding , Ovule/physiology
13.
Am J Bot ; 103(3): 471-83, 2016 Mar.
Article in English | MEDLINE | ID: mdl-26936897

ABSTRACT

PREMISE: Pollen tube growth rate (PTGR) is an important aspect of male gametophyte performance because of its central role in the fertilization process. Theory suggests that under intense competition, PTGRs should evolve to be faster, especially if PTGR accurately reflects gametophyte quality. Oddly, we know remarkably little about how effectively the work of tube construction is translated to elongation (growth and growth rate). Here we test the prediction that pollen tubes grow equally efficiently by comparing the scaling of wall production rate (WPR) to PTGR in three water lilies that flower concurrently: Nymphaea odorata, Nuphar advena and Brasenia schreberi. METHODS: Single-donor pollinations on flower or carpel pairs were fixed just after pollen germination (time A) and 45 min later (time B). Mean PTGR was calculated as the average increase in tube length over that growth period. Tube circumferences (C) and wall thicknesses (W) were measured at time B. For each donor, WPR = mean (C × W) × mean PTGR. KEY RESULTS: Within species, pollen tubes maintained a constant WPR to PTGR ratio, but species had significantly different ratios. N. odorata and N. advena had similar PTGRs, but for any given PTGR, they had the lowest and highest WPRs, respectively. CONCLUSIONS: We showed that growth rate efficiencies evolved by changes in the volume of wall material used for growth and in how that material was partitioned between lateral and length dimensions. The economics of pollen tube growth are determined by tube design, which is consequent on trade-offs between efficient growth and other pollen tube functions.


Subject(s)
Biological Evolution , Nymphaeaceae/growth & development , Pollen Tube/growth & development , Cell Wall/metabolism , Models, Biological , Pollen Tube/anatomy & histology , Regression Analysis , Species Specificity , Temperature
14.
Am J Bot ; 101(4): 559-71, 2014 Apr.
Article in English | MEDLINE | ID: mdl-24663667

ABSTRACT

PREMISE OF STUDY: Male gametophytes of seed plants are sexually immature at the time they are dispersed as pollen, but approximately 30% of flowering plants have tricellular pollen containing fully formed sperm at anthesis. The classic study of Brewbaker (1967: American Journal of Botany 54: 1069-1083) provided a powerful confirmation of the long-standing hypothesis that tricellular pollen had many parallel and irreversible origins within angiosperms. We readdressed the main questions of that study with modern comparative phylogenetic methods. METHODS: We used our own and more recent reports to greatly expand the Brewbaker data set. We modeled trait evolution for 2511 species on a time-calibrated angiosperm phylogeny using (1) Binary State Speciation and Extinction (BiSSE), which accounts for the effect of species diversification rates on character transition rates and, (2) the hidden rates model (HRM), which incorporates variation in transition rates across a phylogeny. KEY RESULTS: Seventy percent of species had bicellular pollen. BiSSE found a 1.9-fold higher bicellular to tricellular transition rate than in the reverse direction, and bicellular lineages had a 1.8-fold higher diversification rate than tricellular lineages. HRM found heterogeneity in evolutionary rates, with bidirectional transition rates in three of four rate classes. CONCLUSIONS: The tricellular condition is not irreversible. Pollen cell numbers are maintained at intermediate frequencies because lower net diversification rates of tricellular lineages are counterbalanced by slower state shifts to the bicellular condition. That tricellular lineages diversify slowly and give rise to bicellular lineages slowly reflects a linkage between the evolution of sporophyte lifestyles and the developmental lability of male gametophytes.


Subject(s)
Biological Evolution , Magnoliopsida/cytology , Pollen/cytology , Magnoliopsida/genetics , Models, Biological , Phylogeny , Pollen/genetics , Species Specificity
15.
AoB Plants ; 2012: pls010, 2012.
Article in English | MEDLINE | ID: mdl-22567221

ABSTRACT

BACKGROUND AND AIMS: The pollination to fertilization process (progamic phase) is thought to have become greatly abbreviated with the origin of flowering plants. In order to understand what developmental mechanisms enabled the speeding of fertilization, comparative data are needed from across the group, especially from early-divergent lineages. I studied the pollen germination process of Austrobaileya scandens, a perennial vine endemic to the Wet Tropics area of northeastern Queensland, Australia, and a member of the ancient angiosperm lineage, Austrobaileyales. METHODOLOGY: I used in vivo and in vitro hand pollinations and timed collections to study development from late pollen maturation to just after germination. Then I compared the contribution of pollen germination timing to progamic phase duration in 131 angiosperm species (65 families). PRINCIPAL FINDINGS: Mature pollen of Austrobaileya was bicellular, starchless and moderately dehydrated-water content was 31.5 % by weight and volume increased by 57.9 % upon hydration. A callose layer in the inner intine appeared only after pollination. In vivo pollen germination followed a logarithmic curve, rising from 28 % at 1 hour after pollination (hap) to 97 % at 12 hap (R(2) = 0.98). Sufficient pollen germination to fertilize all ovules was predicted to have occurred within 62 min. Across angiosperms, pollen germination ranged from 1 min to >60 h long and required 8.3 ± 9.8 % of the total duration of the progamic phase. SIGNIFICANCE: Pollen of Austrobaileya has many plesiomorphic features that are thought to prolong germination. Yet its germination is quite fast for species with desiccation-tolerant pollen (range: <1 to 60 h). Austrobaileya and other early-divergent angiosperms have relatively rapid pollen germination and short progamic phases, comparable to those of many insect-pollinated monocots and eudicots. These results suggest that both the pollen germination and pollen tube growth periods were marked by acceleration of developmental processes early in angiosperm history.

16.
Sex Plant Reprod ; 25(2): 83-96, 2012 Jun.
Article in English | MEDLINE | ID: mdl-22367232

ABSTRACT

Trithuria (Hydatellaceae; Nymphaeales) is unique among early-divergent angiosperms in that its species are extremely small and most have exceptionally short, annual life histories. Given the evolution of these extremes of size and development, we sought to understand whether post-pollination processes still varied predictably with breeding system in Trithuria. To address this question, we studied two Western Australian species, Trithuria austinensis (dioecious, obligately outcrossing) and Trithuria submersa (bisexual, highly selfing). To document developmental timing, carpels were hand-pollinated, collected at sequential time points, and examined with light and fluorescence microscopy. In both species, pollen tubes first entered ovules<1 h after pollination, but the pollen tube pathway of outcrossing T. austinensis was almost four times longer and its pollen tube growth rates were up to six times faster (≤2,166 vs. 321 µm/h) than those of T. submersa. T. austinensis also exhibited greater male investment, slower pollen germination, and greater pollen tube attrition. These differences in male gametophyte development are predicted for outcrossers versus selfers in phylogenetically derived angiosperms. These new data for Hydatellaceae reinforce the idea that an acceleration of pollen tube development occurred in the Nymphaeales stem lineage, before the origin of Hydatellaceae. We infer that a recent evolutionary transition to selfing in T. submersa has been accompanied by predictable modifications to reproductive development, which, because of the ancient relationship between Hydatellaceae and all other angiosperms, suggests that traits underlying the lability of flowering plant post-pollination biology were present early in their history.


Subject(s)
Breeding , Nymphaeaceae/growth & development , Pollen Tube/growth & development , Ecosystem , Flowers/anatomy & histology , Flowers/cytology , Germination/physiology , Glucans/metabolism , Mitosis , Nymphaeaceae/anatomy & histology , Nymphaeaceae/cytology , Pollen Tube/anatomy & histology , Pollen Tube/cytology , Reproduction/physiology , Species Specificity , Time Factors , Western Australia
17.
Evodevo ; 2(1): 14, 2011 Jul 01.
Article in English | MEDLINE | ID: mdl-21722365

ABSTRACT

BACKGROUND: A number of innovations underlie the origin of rapid reproductive cycles in angiosperms. A critical early step involved the modification of an ancestrally short and slow-growing pollen tube for faster and longer distance transport of sperm to egg. Associated with this shift are the predominantly callose (1,3-ß-glucan) walls and septae (callose plugs) of angiosperm pollen tubes. Callose synthesis is mediated by callose synthase (CalS). Of 12 CalS gene family members in Arabidopsis, only one (CalS5) has been directly linked to pollen tube callose. CalS5 orthologues are present in several monocot and eudicot genomes, but little is known about the evolutionary origin of CalS5 or what its ancestral function may have been. RESULTS: We investigated expression of CalS in pollen and pollen tubes of selected non-flowering seed plants (gymnosperms) and angiosperms within lineages that diverged below the monocot/eudicot node. First, we determined the nearly full length coding sequence of a CalS5 orthologue from Cabomba caroliniana (CcCalS5) (Nymphaeales). Semi-quantitative RT-PCR demonstrated low CcCalS5 expression within several vegetative tissues, but strong expression in mature pollen. CalS transcripts were detected in pollen tubes of several species within Nymphaeales and Austrobaileyales, and comparative analyses with a phylogenetically diverse group of sequenced genomes indicated homology to CalS5. We also report in silico evidence of a putative CalS5 orthologue from Amborella. Among gymnosperms, CalS5 transcripts were recovered from germinating pollen of Gnetum and Ginkgo, but a novel CalS paralog was instead amplified from germinating pollen of Pinus taeda. CONCLUSION: The finding that CalS5 is the predominant callose synthase in pollen tubes of both early-diverging and model system angiosperms is an indicator of the homology of their novel callosic pollen tube walls and callose plugs. The data suggest that CalS5 had transient expression and pollen-specific functions in early seed plants and was then recruited to novel expression patterns and functions within pollen tube walls in an ancestor of extant angiosperms.

18.
Ann Bot ; 106(6): 909-20, 2010 Dec.
Article in English | MEDLINE | ID: mdl-21047886

ABSTRACT

BACKGROUND AND AIMS: Trithuria, the sole genus in the family Hydatellaceae, is an important group for understanding early angiosperm evolution because of its sister relationship to the ancient lineage, Nymphaeales (water lilies). Although also aquatic, Trithuria differs from water lilies in that all species are extremely small, and most have an annual life form and grow in seasonal wetlands. Very little is known about their reproductive ecology. This paper reports on reproductive timing, mode of pollination and characteristics of the breeding system of Trithuria submersa in Western Australia. METHODS: Mass collections of open-pollinated plants from different ecological settings were used to characterize the reproductive developmental sequence and natural pollen reception. Hand-pollination, caging and emasculation experiments were used to measure outcross + geitonogamous pollen reception versus autonomous self-pollination in two populations over two field seasons. KEY RESULTS: Natural outcross or geitonogamous pollination was by wind, not by water or insects, but pollen reception was extremely low. Pollen production was very low and pollen release was non-synchronous within populations. The pollen to ovule (P/O) ratio was 23·9, compared with 1569·1 in dioecious Trithuria austinensis. Stigmas became receptive before male phase and remained so until anthers dehisced and autonomous self-pollination occurred. Natural pollen loads are composed primarily of self pollen. Self- and open-pollinated plants had equivalent seed set (both >70 %). Self-pollinated plants produced seed within 17 d. CONCLUSIONS: Autonomous self-pollination and self-fertilization are predominant in T. submersa. The low P/O ratio is not an artefact of small plant size and is inconsistent with long-term pollination by wind. It indicates that T. submersa has evolved a primarily autogamous breeding system. Selfing, along with the effect of small plant size on the speed of reproduction, has enabled T. submersa to colonize marginal ephemeral wetlands in the face of unpredictable pollination.


Subject(s)
Magnoliopsida/physiology , Reproduction/physiology , Breeding , Pollination/physiology , Self-Fertilization/physiology , Western Australia
19.
Am Nat ; 174(1): 13-23, 2009 Jul.
Article in English | MEDLINE | ID: mdl-19422319

ABSTRACT

Fire has been the dominant disturbance in boreal America since the Pleistocene, resulting in a spatial mosaic in which the most fire occurs in the continental northwest. Spatial variation in snowshoe hare (Lepus americanus) density reflects the fire mosaic. Because fire initiates secondary forest succession, a fire mosaic creates variation in the abundance of early successional plants that snowshoe hares eat in winter, leading to geographic variation in hare density. We hypothesize that fire is the template for a geographic mosaic of natural selection: where fire is greatest and hares are most abundant, hare browsing has most strongly selected juvenile-phase woody plants for defense. We tested the hypothesis at multiple spatial scales using Alaska birch (Betula neoalaskana) and white birch (Betula papyrifera). We also examined five alternative hypotheses for geographic variation in antibrowsing defense. The fire-hare-defense hypothesis was supported at transcontinental, regional, and local scales; alternative hypotheses were rejected. Our results link transcontinental variation in species interactions to an abiotic environmental driver, fire. Intakes of defense toxins by Alaskan hares exceed those by Wisconsin hares, suggesting that the proposed selection mosaic may coincide with a geographic mosaic of coevolution.


Subject(s)
Betula/genetics , Betula/metabolism , Ecosystem , Fires , Hares/genetics , Animals , Biological Evolution , Hares/metabolism , Toxins, Biological , Trees , Triterpenes/metabolism
20.
Am J Bot ; 96(1): 144-65, 2009 Jan.
Article in English | MEDLINE | ID: mdl-21628181

ABSTRACT

A remarkable number of the defining features of flowering plants are expressed during the life history stage between pollination and fertilization. Hand pollinations of Amborella trichopoda (Amborellaceae) in New Caledonia show that when the stigma is first receptive, the female gametophyte is near maturity. Pollen germinates within 2 h, and pollen tubes with callose walls and plugs grow entirely within secretions from stigma to stylar canal and ovarian cavity. Pollen tubes enter the micropyle within 14 h, and double fertilization occurs within 24 h. Hundreds of pollen tubes grow to the base of the stigma, but few enter the open stylar canal. New data from Amborella, combined with a review of fertilization biology of other early-divergent angiosperms, show that an evolutionary transition from slow reproduction to rapid reproduction occurred early in angiosperm history. I identify increased pollen tube growth rates within novel secretory carpel tissues as the primary mechanism for such a shift. The opportunity for prezygotic selection through interactions with the stigma is also an important innovation. Pollen tube wall construction and substantial modifications of the ovule and its associated structures greatly facilitated a new kind of reproductive biology.

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