The coexistence of hermaphroditic and dioecious plants is associated with polyploidy and gender dimorphism in Dasiphora fruticosa

Dasiphora fruticosa comprises male,female and hermaphrodite plants,which are distributed sympatrically in some populations on the Qinghai-Tibet Plateau.To explore what governs the coexistence of these three sexual phenotypes,we investigated the DNA contents,pollen and ovule production,pollen deposition,and performed hand-pollination in both hermaphroditic and dioecious individuals of D.fruticosa.Flow cytometry confirmed that the DNA content of males and females were almost twice as much as that of the hermaphrodites.Male and female flowers produced more pollen grains and ovules than hermaphroditic flowers.Hand-pollinated treatments showed that unisexual flowers were sterile in one sexual function and bisexual flowers were fertile for both functions,but no sterile seeds were produced between unisexual and bisexual flowers.Our findings imply that polyploidy is related to gender dimorphism,and both are likely to play a strong role in the coexistence of two cryptic biological species of D.fruticosa(low ploidy hermaphroditic species and high ploidy dioecious species)in the Qinghai-Tibet Plateau.

Identification of a male-specific region(MSR)in Spinacia oleracea

Dioecy,the presence of male and female individual,has evolved independently from hermaphroditism in multiple flowering plant lineages.Spinach,an important leafy vegetable crop worldwide,is a dioecious species with an XY sex-determination system.Although some markers that are fully linked to male-determination locus were identified,the male-specific region(MSR)remained unclear.In this research,five male individuals and five female lines were resequenced to identify the male-specific region.We identified a region(∼21 kb)on chromosome 4(putative sex chromosome)where the five females had a low reads coverage,while the five males had high coverage.A KASP marker,SponR,developed from a single nucleotide polymorphism(SNP)closely linked to the MSR was co-segregating with the sex determination gene in the population of 958 individuals,suggesting that the MSR might be specifically present in male spinach plants.

Rhizosphere microbe populations but not root traits induced by drought in Populus euphratica males

How sex-related root traits and soil microbes and their interactions respond to drought remains unclear.Here,we investigated how fine root traits and the composition of rhizosphere microbial communities in Populus euphratica females and males respond to drought in concert in 17-year-old plantations.Females increased specific root length(SRL)in response to drought.However,males showed no changes in their roots but significant increases in arbuscular mycorrhizal hyphal biomass and population of Gram-negative bacteria in the rhizosphere.Also,fungal symbiotroph communities associated with root systems in males differed from those in females under drought.We further demonstrated that the Gram-positive to Gram-negative bacteria ratios positively correlated with the SRL,while fungi to bacteria ratios were negatively correlated.Meanwhile,the relative abundance of symbiotrophs was negatively correlated with the SRL,while saprotroph abundance was positively correlated.Nevertheless,the relative abundance of symbiotrophs was positively correlated with the root carbon content(RCC).These findings indicate that microbial responses to drought depend highly upon the sex of the plant and microbial group and are related to root trait adjustments to drought.This discovery also highlights the role of plant-microbial interactions in the ecosystems of P.euphratica forest plantations.

Patterns of plant sexual systems in subtropical evergreen broad-leaved forests in Ailao Mountains, SW China

Aims Sexual systems influence many components of the ecology and evolution of plant populations and have rarely been documented in subtropical evergreen broad-leaved forests(SEBLF).Here we report frequency distribution and ecological correlates of plant sexual systems in SEBLF at Ailao Mountains,and compare our results with that of tropical and cool temperate forests.Methods We examine the sexual systems of 703 species of woody angiosperms belonging to 103 families and 296 genera based on a comprehensive survey of SEBLF at Ailao Mountains Natural Reserve.Information of plant sexual systems and ecological traits were mainly based on published literatures and specimens as well as our field observations.The associations between plant sexual system and ecological traits were assessed with chi-square tests.Important findings Among these species,60.2%were hermaphroditic,15.8%were monoecious and 24.0%were dioecious.The percentage of dioecious sexual system among tree species(22.2%)in SEBLF was comparable to those of tropical tree floras,but much higher than those of temperate forests at North America.The percentage of monoecious sexual system among tree species(30.1%)in SEBLF was higher than that of tropical tree floras,but much lower than those of temperate forests at North America.Monoecy was significantly associated with the tree growth form and was relatively common in temperate genera.Dioecy was significantly associated with fleshy fruits and monoecy was significantly associated with dry fruit type in SEBLF.The high percentage of diclinous sexual systems(monoecy and dioecy)in SEBLF may be associated with the origin of the flora and the prevalence of relatively small inconspicuous flowers of the forests in the Oriental Region.

Sexual differences and sex ratios of dioecious plants under stressful environments

Dioecious plants exhibit sexual dimorphism in both sexual features(reproductive organs)and secondary sex characteristics(vegetative traits).Sexual differences in secondary traits,including morphological,physiological and ecological characters,have been commonly associated with trade-offs between the cost of reproduction and other plant functions.Such trade-offs may be modified by environmental stressors,although there is evidence that sexually dimorphic responses to stress do not always exist in all plant species.When sexual dimorphism exists,sexually different responses appear to depend on the species and stress types.Yet,further studies on dioecious plant species are needed to allow the generalization of stress effects on males and females.Additionally,sexual dimorphism may influence the frequency and distribution of the sexes along environmental gradients,likely causing niche differentiation and spatial segregation of sexes.At the present,the causes and mechanisms governing sex ratio biases are poorly understood.This review aims to discuss sex-specific responses and sex ratio biases occurring under adverse conditions,which will advance our knowledge of sexually dimorphic responses to environmental stressors.

Chromosome-level Genomes Reveal the Genetic Basis of Descending Dysploidy and Sex Determination in Morus Plants

Multiple plant lineages have independently evolved sex chromosomes and variable karyotypes to maintain their sessile lifestyles through constant biological innovation.Morus notabilis,a dioecious mulberry species,has the fewest chromosomes among Morus spp.,but the genetic basis of sex determination and karyotype evolution in this species has not been identified.In this study,three high-quality genome assemblies were generated for Morus spp.[including dioecious M.notabilis(male and female)and Morus yunnanensis(female)]with genome sizes of 301–329 Mb and were grouped into six pseudochromosomes.Using a combination of genomic approaches,we found that the putative ancestral karyotype of Morus species was close to 14 protochromosomes,and that several chromosome fusion events resulted in descending dysploidy(2n=2x=12).We also characterized a~6.2-Mb sex-determining region on chromosome 3.Four potential male-specific genes,a partially duplicated DNA helicase gene(named MSDH)and three Ty3_Gypsy long terminal repeat retrotransposons(named MSTG1/2/3),were identified in the Y-linked area and considered to be strong candidate genes for sex determination or differentiation.Population genomic analysis showed that Guangdong accessions in China were genetically similar to Japanese accessions of mulberry.In addition,genomic areas containing selective sweeps that distinguish domesticated mulberry from wild populations in terms of flowering and disease resistance were identified.Our study provides an important genetic resource for sex identification research and molecular breeding in mulberry.

Leaf size versus leaf numbertradeoffs in dioecious angiosperms

Aims We explore the possible role of leaf size/number trade-offs for the interpretation of leaf size dimorphism in dioecious plant species.Methods Total above-ground biomass(both male and female)for three herbaceous dioecious species and individual shoots(from both male and female plants)for three woody dioecious species were sampled to record individual leaf dry mass,number of leaves,dry mass of residual above-ground tissue(all remaining non-leaf biomass),number of flowers/inflorescences(for herbaceous species)and number of branches.Important Findings For two out of three woody species and two out of three herbaceous species examined,male plants produced smaller leaves but with higher leafing intensity—i.e.more leaves per unit of supporting(residual)shoot tissue or plant body mass—compared with females.Male and female plants,however,did not differ in shoot or plant body mass or branching intensity.We interpret these results as possible evidence for a dimorphic leaf deployment strategy that promotes both male and female function,respectively.In male plants,capacity as a pollen donor may be favored by selection for a broadly spaced floral display,hence favoring relatively high leafing intensity because this provides more numerous axillary meristems that can be deployed for flowering,thus requiring a relatively small leaf as a trade-off.In one herbaceous species,higher leafing intensity in males was associated with greater flower production than in females.In contrast,in female plants,selection favors a relatively large leaf,we propose,because this promotes greater capacity for localized photosynthate production,thus supporting the locally high energetic cost of axillary fruit and seed development,which in turn requires a relatively low leafing intensity as a trade-off.

Sex-specifically responsive strategies to phosphorus availability combined with different soil nitrogen forms in dioecious Populus cathayana

Aims Phosphorus(P)availability and efficiency are especially important for plant growth and productivity.However,the sex-specific P acquisition and utilization strategies of dioecious plant species under different N forms are not clear.Methods This study investigated the responsive mechanisms of dioecious Populus cathayana females and males based on P uptake and allocation to soil P supply under N deficiency,nitrate(NO3−)and ammonium(NH4+)supply.Important Findings Females had a greater biomass,root length density(RLD),specific root length(SRL)and shoot P concentration than males under normal P availability with two N supplies.NH4+supply led to higher total root length,RLD and SRL but lower root tip number than NO3−supply under normal P supply.Under P deficiency,males showed a smaller root system but greater photosynthetic P availability and higher leaf P remobilization,exhibiting a better capacity to adaptation to P deficiency than females.Under P deficiency,NO3−supply increased leaf photosynthesis and P use efficiency(PUE)but reduced RLD and SRL in females while males had higher leaf P redistribution and photosynthetic PUE than NH4+supply.Females had a better potentiality to cope with P deficiency under NO3−supply than NH4+supply;the contrary was true for males.These results suggest that females may devote to increase in P uptake and shoot P allocation under normal P availability,especially under NO3−supply,while males adopt more efficient resource use and P remobilization to maximum their tolerance to P deficiency.

Neither Biased Sex Ratio nor Spatial Segregation of the Sexes in the Subtropical Dioecious Tree Eurycorymbus cavaleriei(Sapindaceae)

Knowledge of sex ratio and spatial distribution of males and females of dioecious species is both of evolutionary interest and of crucial importance for biological conservation. Eurycorymbus cavaleriei, the only species in the genus Eurycorymbus （Sapindaceae）, is a dioecious tree endemic to subtropical montane forest in South China. Sex ratios were investigated in 15 natural populations for the two defined ages （young and old）. Spatial distribution of males and females was further studied in six large populations occurring in different habitats （fragmented and continuous）. The study revealed a slight trend of male- biased sex ratio in both ages of E. cavaleriei, but sex ratio of most populations （13 out of 15） did not display statistically significant deviation from equality. All of the four significantly male-biased populations in the young class shifted to equality or even female-biased, The Ripley＇s K analysis of the distribution of males with respect to females suggested that individuals of the opposite sexes were more randomly distributed rather than spatially structured. These results suggest that the male-biased sex ratio in E. cavaleriei may result from the precocity of males and habitat heterogeneity. The sex ratio and the sex spatial distribution pattern are unlikely to constitute a serious threat to the survival of the species.

Gender plasticity uncovers multiple sexual morphs in natural populations of Cedrus deodara (Roxb.) G. Don

Background:The expression of gender in gymnosperms is challenging because the extent of variability in gender segregations in tree crowns and selection pressure of nature can modify the gender through time.Methods:An in-depth investigation on spatial segregation of genders in tree crowns and sex expression of a total of 500 trees in five different natural populations of Cedrus deodara was carried out and verified the occurrence of subdioecious(co-existence of male,female,and monoecious)genders in C.deodara.Results:Five different sexual morphs were apparent among the 500 selected individuals as(1)pure male(M):bearing only male strobili in the whole crown with 22.2%;(2)pure female(F):bearing only female strobili in the whole crown with 12.4%;(3)mixed-monoecious(MM):bearing both male and female strobili with 13.6%;(4)predominantly female(PF)with 25.6%;and(5)predominantly male(PM)with 26.2%.The occurrence of multiple sexual morphs resulted from the complex selection pressure,which increased the stability of the populations.The segregation of genders in crown layers deemed to increase the fitness that may be a mechanism for accelerating outcrossing.The results of the study suggest that the subdioecious gender expression in C.deodara is evolved through the monoecy–paradioecy pathway.The production of male strobili revealed non-significant effect of tree sizes whereas a significant effect was observed for the production of female strobili.Our study established that the total pollen and seed outputs in C.deodara changed frequently according to gender expression.Conclusions:The size of the tree,resource availability,sex allocation,plant architecture,gender segregation in crowns,and habitat conditions are the prominent causes for gender plasticity.

Floral biology and pollination mechanisms of four Mexico-endemic Fuchsia species with contrasting reproductive systems

Aims The evolution of the outstanding variation of reproductive systems in angiosperms has been considered an important driver of line-age diversification.Closely related hermaphroditic and dioecious species with biotic pollination provide the opportunity to study and compare traits related to pollinator attraction and their con-sequences on reproductive components.A higher predictability of pollination syndromes is expected in dioecious species,which are dependent on pollinators,than in self-compatible hermaphroditic taxa.Dioecious species may suffer pollen limitation depending on the quality of floral rewards and the kind and abundance of pollina-tors,whereas no pollen limitation is expected in hermaphroditic spe-cies with autonomous self-pollination.Additionally,in the absence of pollen limitation,more or better seeds are expected in dioecious species,according to the sexual specialization hypothesis.Methods In natural populations of the hermaphroditic Fuchsia fulgens and Fuchsia arborescens and dioecious Fuchsia parviflora and Fuchsia obconica,all endemic to Mexico,we first described flower phenol-ogy,flower production and longevity and nectar volume and concen-tration.Then,we evaluated the correspondence between floral visitors and pollination syndromes.In hermaphrodite plants,we determined the level of herkogamy and the potential for autonomous self-pollina-tion.Finally,we evaluated the effect of pollen limitation on fruit set and seed number and assessed seed germination for all species.Important Findings In contrast to our prediction,dioecious species did not show a higher correspondence between pollination syndromes and floral visitors than did hermaphrodites;however,male flowers exhib-ited a higher correspondence than female flowers.No pollen limitation was detected in dioecious species,for which visitation rate did not differ between male and female flowers.The her-maphroditic F.fulgens showed pollen limitation for seed number,despite the presence of autonomous selfing.Fruit set from auton-omous pollination was higher in F.arborescens,which showed a lower level of herkogamy compared with F.fulgens.Finally,dioecious species produced fewer but heavier seeds compared with hermaphrodite species.Although Fuchsia is classified as an outcrossing genus,both hermaphroditic species showed autono-mous self-pollination.The heavier but lower number of seeds per fruit in dioecious species may be related to the more efficient resource allocation expected from sexual specialization.This could play an important role in the evolution of dioecy;however,a comparative phylogenetic approach is required to confirm this hypothesis.