Why does some pollen lack apertures? A review of inaperturate pollen in eudicots

Apertures are key characters of pollen grains with systematic importance in angiosperms. They function as sites for pollen tube exit, water uptake, transfer of recognition substances and accommodation of volume changes. Not all pollen has apertures; inaperturate pollen (lacking obvious apertures) characterizes many angiosperm groups, especially in early divergent angiosperms and monocots, but also eudicots. In order to expand our knowledge of the systematic distribution, possible functional significance and development of inaperturate pollen in angiosperms, this review focuses on inaperturate and cryptoaperturate (with hidden apertures) pollen in the large eudicot clade, which comprises about 75% of present‐day angiosperm species. It includes new TEM observations of inaperturate pollen from four exemplar taxa selected from different parts of the eudicot phylogeny. Two categories of inaperturate (including cryptoaperturate) pollen occur in eudicots. (1) Sterile attractant or feeding pollen associated with functional dioecy has evolved iteratively at least six times in conjunction with complex breeding systems in the core eudicots. (2) Fertile pollen has evolved numerous times independently throughout eudicots, though generally in a relatively small number of individual taxa. Notable exceptions are the petaliferous crotonoid Euphorbiaceae s.s., in which fertile inaperturate pollen occurs in c. 1500 species, and two subfamilies of Apocynaceae s.l. (Secamonoideae and Asclepiadoideae) with c. 2500 species with fertile inaperturate pollen in pollinia. Fertile inaperturate pollen is sometimes (but not always) associated with an aquatic habit, parasitism, insectivory, heterostyly, anemophily or pollinia. Most fertile inaperturate pollen has a thin exine, or the exine is largely restricted to isolated components (muri, protuberances, subunits) separated by thinner areas which probably function as apertures. In cryptoaperturate pollen, the aperture is covered by continuous exine which probably has a protective function, similar to an operculum. Developmentally, inaperturate pollen is not associated with any particular tetrad type or meiotic spindle orientation (unlike some apertures) due to the absence of a colpal shield of endoplasmic reticulum or other organelles and hence is independent of microsporogenesis type. The lack of a colpal shield during the tetrad stage of development permits complete deposition of first primexine and then exine around each microspore, possibly mediated by the action of the DEX1 protein. © 2007 The Linnean Society of London, Botanical Journal of the Linnean Society, 2007, 155 , 29–48.     

Intergeneric pollen – megagametophyte relationships of conifers in vitro

 Germinating pollen from larch (Larix occidentalis), Sitka spruce (Picea sitchensis) and white pine (Pinus monticola) were co-cultured with megagametophytes dissected from cones of other genera (Pseudotsuga menziesii, Larix×eurolepis and Pinus monticola). Pollen was presented to megagametophytes possessing archegonia which were either alive, degenerating or dead. In addition, pollen was presented to fertilized megagametophytes and to megagametophytes that had been cut in half. Megagametophyte penetration by pollen tubes and male gamete release into archegonia were verified by serial sections of glycomethacrylate-embedded specimens. Pollen tubes penetrated through any part of the apex of the megagametophyte. Division of the body cell into the two gametes was regularly observed. Delivery of gametes was confirmed between spruce and larch. Pollen tubes also penetrated fertilized megagametophytes, dead or degenerating archegonia as well as wounded and/or cut surfaces. This demonstrates the inability of the male gametophyte to optimize its mating efforts, since it is unable to differentiate between healthy and unhealthy archegonia. The megagametophyte cells are unable to optimize male selection. They may produce secretions of a generally attractive nature, as pollen is attracted to the apex of the megagametophyte, but archegonia themselves do not produce pollen-specific signals of either a promotive or inhibitory nature. These results open new avenues for the development of novel breeding strategies where natural breeding barriers may be bypassed. Received: 19 March 1998 / Accepted: 29 April 1998     

Airborne pollen in Bahía Blanca,Argentina: seasonal distribution of pollen types

The composition and seasonal distribution of airborne pollen grains in the atmosphere of Bahía Blanca, Argentina, has been studied between June 2001 and December 2003 using the Rotorod sampler (model 40). The results show that the main pollen types during this period were Cupressaceae, Fraxinus, Myrtaceae, Poaceae, Amaranthus/Chenopodiaceae, Pinus, Urticaceae, Ulmus, Olea and Styphnolobium. The highest concentrations occurred from August to December (end of winter and spring), accounting for 80% of the total annual pollen count. The greatest diversity was found in the spring, with the major of pollen coming from short-flowering plant types, such as Populus, Acer, Platanus, Juglans, Tamarix, Ailanthus and Typha. The potential sources of pollen from woody ornamental species are Cupressus sempervirens, Eucalyptus camaldulensis and Fraxinus pennsylvanica. whereas those from herbaceous species are the Chenopodiaceae and Poaceae, which are found within the city and also in the surrounding natural vegetation, and the Urticaceae, which are only present in the city. Marked annual differences were noted during the study period. The increase in 2002 may have been due to the abundant rainfall that occurred prior to the spring season, which would have favored the vegetative stage and flower development of plants. The decrease in pollen concentration in 2003 was mainly due to low rainfall throughout the year.     

Variation in annual pollen accumulation rates of Fagus along a N–S transect in Europe based on pollen traps

Annual pollen-accumulation rates (PAR) of Fagus (beech) obtained within the framework of the Pollen Monitoring Programme (PMP) were analyzed in pollen traps along a N–S transect from the Baltic Sea to the Black Sea in different European vegetation units. The study regions are situated in the lowlands of northern Poland, the uplands of SE Poland, the Czech Krkono?e Mts, the Czech ?umava Mts, the Swiss Jura Mts, the Swiss Alps, the Bulgarian Rila Mts and the Bulgarian Strandzha Mts. Most time series are 10 or 11 years long, some are 5–16 years long. Inter-annual fluctuations in Fagus PAR were analyzed and compared with seed mast years. Years with high Fagus PAR and others with low Fagus PAR occurred most frequently in parallel within each region and often in two neighbouring regions. 2006 was exceptional as it had a very high Fagus sylvatica pollen deposition in all study regions and it was also a mast year. In Bulgaria, the trend in the 5 years of Fagus orientalis PAR in the Strandzha Mts differed from that of F. sylvatica PAR in the Rila Mts. Aiming at establishing the relationship between average Fagus PAR and tree cover, differences in Fagus PAR (averaged per pollen trap) were related in each region to the proportion of beech trees in the vegetation within 2 km of the pollen traps, the distance to the nearest pollinating Fagus tree, regional or local presence of beech forests, the degree of landscape openness, and the size of forest opening in which a trap is situated. Average Fagus PAR was found to track the regional abundance of beech trees in the vegetation, not the distance of the nearest Fagus tree. Regional occurrence of beech-dominated forests was reflected by a Fagus PAR of ca. 1,400 grains cm^?2 year^?1, local abundance very close to pollen traps by ca. 2,400 grains, small patches of forest with admixture of Fagus by ca. 170–220 grains, and scarcity or absence of Fagus by ca. 40 grains or less.     

Structural analysis of stigma development in relation with pollen–stigma interaction in sunflower

Structural analysis of stigma development in sunflower highlights the secretory role of papillae due to its semi-dry nature. Production of lipid-rich secretions is initiated at the staminate stage of the flowers in stigma development and increases at the receptive stage, coinciding with an extensive development of elaioplasts and endoplasmic reticulum network in the basal region of the papillae. Transfer cells, earlier identified only in the wet type of stigma, are also present in the transmitting tissue of the sunflower stigma. Attainment of physiological maturity by the stigmatic tissue, accompanying development from bud to pistillate stage, appears to affect the initial steps of pollen–stigma interaction. The nature of self-incompatibility in Helianthus has also been investigated in relation with pollen adhesion, hydration and germination. Pollen adhesion to the stigma is a rapid process in sunflower and stigma papillae exhibit greater affinity for pollen during cross pollination as compared to self-pollination. Components of the pollen coat and the pellicle on the surface of stigmatic papillae are critical for the initial phase of pollen–stigma interaction (adhesion and hydration). The lipidic components of pollen coat and the proteinaceous and lipidic components from the surface of the papillae coalesce during adhesion, leading to the movement of water from stigma to the pollen, thereby causing pollen hydration and its subsequent germination. Pollen germination (both in self-and cross-pollen) on the stigma surface and the growth of the pollen tube characterize the flexibility of self-incompatibility in sunflower. Compatible pollen grains germinate and the pollen tube penetrates the stigma surface to enter the nutrient-rich transmitting tissue. The pollen tube from incompatible pollen germination, however, fails to penetrate the stigmatic tissue and it grows parallel to the papillae. Present findings provide new insights into structural and functional relationships during stigma development and pollen–stigma interaction.     

Airborne pollen of Ambrosia in Burgundy (France) 1996–1997

Pollen counts in Burgundy were monitored by means of four Hirst volumetric traps. Their analysis revealed a sharp rise of Ambrosia from 1996 to 1997. The minimum amount of ragweed pollen likely to provoke allergies (13 grains m–3) was reached or exceeded several days every year, but without leading to clinical symptoms. The circadian variation of Ambrosia pollen showed two peaks: the first one in the morning was suggested to coincide with local pollination, although the second one, in the afternoon, seemed to result from a long range transport which was confirmed by the study of wind roses.     

A practical approximation of pollen dispersal–deposition for calculation of pollen productivity and quantification of vegetation

We compared simple mathematical pollen dispersal–deposition models with Gaussian plume models. The simple mathematical models proved equal or better approximations of real world pollen dispersal–deposition. We concluded that for most standard applications, such as estimating pollen productivity or quantitative vegetation reconstructions, simple mathematical models would perform satisfactory. Such easy-to-use models may lower the threshold to employ quantitative tools to palaeoecological questions.     

Histoenzymological compartmentation of β-glucuronidase in the germinating pollen grains ofPortulaca grandiflora

The contribution deals with the distribution of β-glucuronidase in the germinating pollen grains ofPortulaca grandiflora. In non-germinating pollen grains the enzyme is localized in the pollen wall; the cytoplasmic activity is subdued. With the initiation of germination, the activity of enzyme increases and the positive granules are richly packed in the pollen grains and pollen tubes. The stigma hairs also have such an activity. The functions of the enzyme in the metabolism of germinating pollen grains are discussed.     

Immuno-gold localization of α-L-arabinofuranosyl residues in pollen tubes of Nicotiana alata Link et otto

Immuno-gold labelling using a monoclonal antibody (PCBC3) with a primary specificity for -L-arabinofuranosyl residues was used to locate these residues in pollen tubes of Nicotiana alata grown in vivo. The antibody bound to the outer fibrillar layer of the pollen-tube wall: the inner, non-fibrillar wall layer was not labelled. Cytoplasmic vesicles (0.2 m diameter) were also labelled. The antibody may bind to an arabinan in the pollen-tube wall.     

Trends in atmospheric concentrations of weed pollen in the context of recent climate warming in Poznań (Western Poland)

A significant increase in summer temperatures has been observed for the period 1996–2011 in Poznań, Poland. The phenological response of four weed taxa, widely represented by anemophilous species (Artemisia spp., Rumex spp. and Poaceae and Urticaceae species) to this recent climate warming has been analysed in Poznań by examining the variations in the course of airborne pollen seasons. Pollen data were collected by 7-day Hirst-type volumetric trap. Trends in pollen seasons were determined using Mann–Kendall test and Sen’s slope estimator, whereas the relationships between meteorological and aerobiological data were established by Spearman’s rank correlation coefficient. Significant trends in pollen data were detected. The duration of pollen seasons of all analysed taxa increased (from +2.0 days/year for Urticaceae to +3.8 days/year for Rumex), which can be attributed to a delay in pollen season end dates rather than earlier start dates. In addition, the intensity of Artemisia pollen seasons significantly decreased and correlates with mean July–September daily minimum temperatures (r?=??0.644, p?Rumex pollen seasons. The results of this study show that observed shifts in weed pollen seasons in Poznań, i.e. longer duration and later end dates, might be caused by the recorded increase in summer temperature. This influence was the strongest in relation to Artemisia, which is the taxon that flowers latest in the year. The general lack of significant correlations between Rumex and Urticaceae pollen seasons and spring and/or summer temperature suggests that other factors, e.g. land use practices, could also be partially responsible for the observed shifts in pollen seasons.     

Localization of pectins in the pollen tube wall of Ornithogalum virens L. Does the pattern of pectin distribution depend on the growth rate of the pollen tube?

Monoclonal antibodies that recognize pectins were used for the localization of esterified (JIM7) and acidic, unesterified (JIM5) forms of pectin in pollen tube walls of Ornithogalum virens L. (x = n = 3). The results indicated that the distribution of the two forms of pectin in the pollen tube wall depended on the medium (liquid or solid) used for pollen germination. In pollen tubes grown in the liquid medium, the localization of JIM7 was limited to the very tip of the pollen tube, whereas the localization of JIM5 indicated a uniform distribution of unesterified pectins in the very tip of the tube and along the subapical parts of the tube wall. In tubes germinated on the medium stabilized with agar (1–2%) the localization of JIM7 and JIM5 indicated the presence of both forms of pectin in the tube tip and along the whole length of the pollen tube wall in a ring-like pattern. Thus, the localization of esterified pectins in the sub-apical part of the pollen tube wall, below the apex of the tube, is described for the first time. Measurements of the growth rates of pollen tubes growing on the two types of medium indicated that oscillations in tube growth rate occur but these do not coincide with the pattern of pectin distribution in the tube wall. Our results complement the previous data obtained for the localization of JIM5 and JIM7 in pollen tube walls of other plant species. (Y.-Q. Li et al. 1994, Sex Plant Reprod 7: 145–150) and provide new insight into an understanding of the construction of the pollen tube wall and the physiology of pollen grain germination. Received: 25 January 1999 / Accepted: 23 June 1999     

Cyclic pollen production in Cedrus deodara

Based on a seven-year study of pollen production and release in two different natural populations of Cedrus deodara from Garhwal Himalaya, India, we determined that pollen output follows a two-year cycle. Pollen productivity determinations considered various sources of variability, including the number of pollen strobili per branch, strobili per tree, microsporophylls per tree and pollen grains per tree. Each of these parameters revealed significant year-to-year and population effects. Microsporangium dehiscence took from 2.5 to 3.5 days. Maximum dehiscence was observed between 12:00 and 14:00 h, which coincides with diurnal highest temperature and lowest relative humidity. Annual production of pollen per tree varied from averages of 4.7 × 10⁹, 7.2 × 10⁹ and 5.1 × 10⁹ in years of low production, with alternate high years, producing 12.6 × 10⁹, 14.1 × 10⁹, 13.3 × 10⁹ and 14.0 × 10⁹ pollen grains per tree. Annual pollen production in individual trees of C. deodara ranged from 1.4 × 10⁹ to 22.3 × 10⁹.     

Annual variation of airborne pollen in the city of Palencia,Spain, 1990–1992

The aim of this work is to present the atmospheric pollen concentrations of Palencia, Spain. Data were collected for three consecutive years (1990–92). An active volumetric pollen trap, type CAP2, was used. During this time, 88 different pollen types were identified, of which 27 occured at more than 0.15% of the total pollen recorded annually. These types formed the main pollen spectrum of this sampling station. Pollen coming from herbs (Poaceae, Chenopodiaceae, Plantago Urticaceae, etc.) was predominant (53.79%); arboreal pollen (Quercus, Populus Cupressaceae, etc.) represented 42.11%, and pollen from shrubs (Ericaceae, Sambucus etc.) only 4.10%.

May and June was the time of the year with maximum pollen emission to the air. This was due to the quantities of pollen coming from Poaceae and Quercus which together represent 47.25% of the pollen recorded over the three‐year sampling period. Herbaceous pollen appeared throughout the year with maximum concentrations recorded in the spring, coinciding with the maximum levels of arboreal pollen in the atmosphere.

An analysis of multiple regression and one‐way anova test between pollen concentrations and selected meteorological parameters show that relative humidity and average temperature are the meteorological factors most correlated with the concentrations of specific pollen types (Plantago, Ligustrum, Sambucus, Carex). In the same way, when the winds are predominantly from the northeast (second quadrant), there are higher pollen concentrations of Sambucus Ericaceae and Mercurialis.     

Trends in airborne pollen: An overview of 21 years of data in Neuchâtel (Switzerland)

Airborne pollen analysis has been carried outin Neuchâtel (Switzerland) since 1979. Inthe context of increasing prevalence of pollenallergies and global climate warming, thisstudy attempts to confirm whether airbornepollen may be responsible for the former orindicative of the latter, and presents somegeneral features of pollen flight in westernSwitzerland. The most common pollen types are Taxus/Cupressaceae, Quercus, Poaceae, Pinus,Betula, Urticaceae and Fraxinus. Duringthe 21 years studied, there was no major changein the abundance of pollen. Among thetwenty-five taxa studied only five presented asignificant trend: an increase of pollenquantities was observed for Alnus,Ambrosia, Artemisia and Taxus/Cupressaceae and a decrease for Ulmus. The plant species flowering in winterand in spring were influenced by the mildwinters of the 1990s: 71% of the dates of theonset or the end of the pollen seasons nowadaysoccur significantly earlier in the year. Theobserved advance reaches 0.84 days/year. Treesappear to react stronger to the climate changethan grass and weeds. No pollen type present aprolonged season, so the trend appears to betowards a shift in the timing of pollenpresence in the air. These observations show that the main cause ofthe spectacular increase of pollinosisprevalence in industrialised countries isprobably not to be found in the weak tendencytowards a rise of pollen abundance, except forsome particular pollen types which can broadenthe spectra and/or intensify the abundance ofmajor allergens present in an area. However,airborne pollen is confirmed to be a sensitiveindicator of climate change. The observedshifts in the pollen seasons make necessary theadequate information for people concerned withpollen allergies, in particular for preventionand therapy purposes.     

Is reproduction of endemic plant species particularly pollen limited in biodiversity hotspots?

Current evidence suggests that plants in biodiversity hotspots suffer more from pollen limitation of reproduction than those in lower diversity regions, primarily due to the response of self‐incompatible species. Species in biodiversity hotspots may thus be more at risk of limited reproduction and subsequent population decline. Should these species have restricted ranges (i.e. be endemics to a certain region), pollen limitation within highly diverse regions may pose an important threat to global plant biodiversity. We further dissect the global pattern by exploring whether pollen limitation of range‐restricted (endemic) species is distinctive and/or relates differently to species diversity than that of widespread (non‐endemic) species. To provide a preliminary test of this prediction we conducted both cross‐species and comparative phylogenetic meta‐analyses to determine the effect of endemism on the magnitude of pollen limitation and its relationship with regional species richness. Our data set included 287 plant species belonging to 78 families distributed world‐wide. Our results revealed that endemism and self‐compatibility contribute to the global association between pollen limitation and species richness. Self‐incompatible species were more pollen limited than self‐compatible ones, and the PICs analysis indicated that transitions to endemism were associated with transitions to self‐compatibility. The relationship between pollen limitation and species richness was significant only for the self‐incompatible species, and was monotonically increasing in non‐endemic species but accelerating in the endemic species. Thus, self‐incompatible endemic species from biodiversity hotspots are at the greatest risk of pollination failure, a previously unknown aspect suggesting this group of species as a top priority for future development of conservation strategies. In contrast, reproduction of self‐compatible species appears to be unrelated to plant diversity, although we caution that current data do not account for the reproductive limitation due to the quality of pollen received. Understanding the mechanisms underlying these patterns requires further investigation into plant–plant pollinator mediated interactions and the dynamics of pollen transfer in communities differing in species diversity.     

The promoter of aBrassica napus polygalacturonase gene directs pollen expression ofβ-glucuronidase in transgenicBrassica plants

A 647-bp 5-flanking fragment obtained from genomic clone Sta 44G(2) belonging to a family of polygalacturonase genes expressed inBrassica napus pollen was fused to the-glucuronidase (GUS) marker gene. This fusion construct was introduced intoB. napus plants viaAgrobacterium tumefaciens transformation. Analysis of the transgenicB. napus plants revealed that this promoter fragment is sufficient to direct GUS expression specifically in the anther and that GUS activity increases in pollen during maturation.Abbreviation GUS -Glucuronidase     

Poaceae pollen in the atmosphere of Zagreb (Croatia), 2002 – 2005

Pollen of grasses (Poaceae) is one of the most important airborne allergen sources worldwide. The aim of the study was to determine diurnal, day‐to‐day, weekly, monthly and annual pollen variation, and the effect of selected meteorological parameters on atmospheric pollen concentrations in Zagreb. A preliminary study was carried out during four seasons (2002 – 2005), using a 7‐day VPPS 2000 Hirst volumetric pollen trap. Total annual grass pollen concentrations in Zagreb were constant (2 673 – 3 074 p.g.m^?3), with a relative drop in 2004 (1 196 p.g.m^?3). The beginning of the grass pollen season is usually observed when the average daily temperature exceeds 13.5°C (max. daily temp. 19.5°C), without precipitation. In all four study years the absolute peak of concentrations occurs in the second half of May. The length of pollen season during the study period was 157 – 173 days. A high variability was observed in the maximal concentration and in the number of days when grass pollen concentration exceeded the threshold value of 30 p.g.m^?3 (9 – 40 days). Statistically significant correlations were found between airborne grass pollen concentrations and air temperature, level of precipitation and relative humidity.     

Analysis of the tip-to-base gradient of CaM in pollen tube pulsant growth using in vivo CaM–GFP system

Ca²⁺-CaM signaling is involved in pollen tube development. However, the distribution and function of CaM and the downstream components of Ca²⁺-CaM signal in pollen tube development still need more exploration. Here we obtained the CaM–GFP fusion protein transgenic line of Nicotiana tobacum SRI, which allowed us to monitor CaM distribution pattern in vivo and provided a useful tool to observe CaM response to various exogenous stimulations and afforded solid evidences of the essential functions of CaM in pollen tube growth. CaM–GFP fusion gene was constructed under the control of Lat52-7 pollen-specific promoter and transformed into Nicotiana tobacum SRI. High level of CaM–GFP fluorescence was detected at the germinal pores and the tip-to-base gradient of fluorescence was observed in developing pollen tubes. The distribution of CaM at apical dome had close relationship with the pulsant growth mode of pollen tubes: when CaM aggregated at the apical dome, pollen tubes stepped into growth state; When CaM showed non-polarized distribution, pollen tubes stopped growing. In addition, after affording exogenous Ca²⁺, calmidazolium (antagonism of CaM) or Brefeldin A (an inhibitor of membrane trafficking), CaM turned to a uniform distribution at the apical dome and pollen tube growth was held back. Taken together, our results showed that CaM played a vital role in pollen tube elongation and growth rate, and the oscillation of tip-to-base gradient of CaM was required for the normal pulsant growth of pollen tube.