Isoetes

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Isoetes
Temporal range: Jurassic–Recent
Isoetes tegetiformans.jpg
Isoetes tegetiformans with U.S. penny for scale
Scientific classification OOjs UI icon edit-ltr.svg
Kingdom: Plantae
Clade: Tracheophytes
Clade: Lycophytes
Class: Lycopodiopsida
Order: Isoetales
Family: Isoetaceae
Genus: Isoetes
L.
Species

See text

Isoetes, commonly known as the quillworts, is a genus of lycopod. It is the only living genus in the family Isoetaceae and order Isoetales. There are currently 192 recognized species, [1] with a cosmopolitan distribution mostly in aquatic habitats but with the individual species often scarce to rare. Some botanists split the genus, separating two South American species into the genus Stylites, although molecular data place these species among other species of Isoetes, so that Stylites does not warrant taxonomic recognition. [2] Species virtually identical to modern quillworts have existed since the Jurassic epoch, [3] though the timing of the origin of modern Isoetes is subject to considerable uncertainty. [4]

Contents

The name of the genus may also be spelled Isoëtes. The diaeresis (two dots over the e) indicates that the o and the e are to be pronounced in two distinct syllables. Including this in print is optional; either spelling (Isoetes or Isoëtes) is correct. [5]

Description

Quillwort megasporangia Isoetes megasporangia L.jpg
Quillwort megasporangia

Quillworts are mostly aquatic or semi-aquatic in clear ponds and slow-moving streams, though several (e.g. I. butleri , I. histrix and I. nuttallii ) grow on wet ground that dries out in the summer. The quillworts are spore-producing plants and highly reliant on water dispersion. Quillworts have different ways to spread their spores based on the environment. Quillwort leaves are hollow and quill-like, with a minute ligule at the base of the upper surface. [6] : 7  arising from a central corm. The sporangia are sunk deeply in the leaf bases. Each leaf will either have many small spores or fewer large spores. Both types of leaf are found on each plant. [7] Each leaf is narrow, 2–20 centimetres (0.8–8 in) long (exceptionally up to 100 cm or 40 in) and 0.5–3.0 mm (0.02–0.12 in) wide; they can be either evergreen, winter deciduous, or dry-season deciduous. Only 4% of total biomass, the tips of the leaves, is chlorophyllous. [8]

The roots broaden to a swollen base up to 5 mm (0.2 in) wide where they attach in clusters to a bulb-like, underground rhizome characteristic of most quillwort species, though a few (e.g. I. tegetiformans ) form spreading mats. This swollen base also contains male and female sporangia, protected by a thin, transparent covering (velum), which is used diagnostically to help identify quillwort species. They are heterosporous. Quillwort species are very difficult to distinguish by general appearance. The best way to identify them is by examining their megaspores under a microscope. Moreover, habitat, texture, spore size, and velum provide features that distinguish Isoëtes taxa. [9] They also possess a vestigial form of secondary growth in the basal portions of its cormlike stem, an indication that they evolved from larger ancestors. [10]

Biochemistry and genetics

Quillworts use Crassulacean acid metabolism (CAM) for carbon fixation. Some aquatic species don't have stomata and the leaves have a thick cuticle which prevents CO2 uptake, a task that is performed by their hollow roots instead, which absorb CO2 from the sediment. [11] This has been studied extensively in Isoetes andicola. [8] CAM is normally considered an adaptation to life in arid environments to prevent water loss with the plants opening their stomata at night rather than in the heat of the day. This allows CO2 to enter and minimises water loss. As mostly submerged aquatic plants, quillworts do not lack water and the use of CAM is considered to avoid competition with other aquatic plants for CO2 during daytime. [12]

The first detailed quillwort genome sequence, of I. taiwanensis , [13] showed that there were differences from CAM in terrestrial plants. CAM involves the enzyme phosphoenolpyruvate carboxylase (PEPC) and plants have two forms of the enzyme. One is normally involved in photosynthesis and the other in central metabolism. From the genome sequence, it appears that in quillworts, both forms are involved in photosynthesis. In addition, the time of day of the peak abundance of some of the components of CAM was different from terrestrial plants. These fundamental differences in biochemistry suggests that CAM in quillworts is probably another example of convergent evolution of CAM during the more than 300 million years since the genus diverged from other plants. However, they may also be because of differences between life in water and in the air. [13] The genome sequence also provided two insights into its structure. First, genes and repeated non-coding regions were fairly evenly distributed across all the chromosomes. This is similar to genomes of other non-seed plants, but different from the seed plants (angiosperms) where there are distinctly more genes at the ends of chromosomes. Secondly, there was also evidence that the whole genome had been duplicated in the ancient past. [13]

Reproduction

Reproductive cycle of Isoetes Isoetes.reproduction.tif
Reproductive cycle of Isoetes

Overview

Like all land plants, Isoetes undergoes an alternation of generations between a diploid sporophyte stage and a sexual haploid gametophyte stage. However, the dominance of one stage over the other has shifted over time. The development of vascular tissue and subsequent diversification of land plants coincides with the increased dominance of the sporophyte and reduction of the gametophyte. Isoetes, as members of the Lycopodiopsida class, are part of the oldest extant lineage that reflects this shift to a sporophyte dominant lifecycle. In closely related lineages, such as the extinct Lepidodendron , spores were dispersed by the sporophyte through large collections of sporangia called strobili for wind-based spore dispersal. [14] However, Isoetes are small heterosporous semi-aquatic plants, with different reproductive needs and challenges than large tree-like land plants.

Description

Like the rest of the Lycopodiopsida class, Isoetes reproduces with spores. [15] Among the lycophytes, both Isoetes and the Selaginellaceae (spikemosses) are heterosporous, while the remaining lycophyte family Lycopodiaceae (clubmosses) is homosporous. [16] As heterosporous plants, fertile Isoetes sporophytes produce megaspores and microspores, which develop in the megasporangia and microsporangia. [17] These spores are highly ornate and are the primary way by which species are identified, although no one functional purpose of the intricate surface patterns is agreed upon. [18] The megasporangia occur within the outermost microphylls (single-veined leaves) of the plant while the microsporangia are found in the innermost microphylls. [19] This pattern of development is hypothesized to improve the dispersal of the heavier megaspore. [15] These spores then germinate and divide into mega- and micro- gametophytes. [17] [20] [21] The microgametophytes have antheridia, which in turn produce sperm. [21] The megagametophytes have archegonia, which produce egg cells. [21] Fertilization takes place when the motile sperm from a microgametophyte locates the archegonia of a megagametophyte and swims inside to fertilize the egg.

Outside of heterospory, a distinguishing feature of Isoetes (and Selaginella ) from other pteridophytes, is that their gametophytes grow inside the spores. [17] [21] [19] This means that the gametophytes never leave the protection of the spore that disperses them, cracking the perispore (the outer layer of the spore) just enough to allow the passage of gametes. This is fundamentally different from ferns, where the gametophyte is a photosynthetic plant exposed to the elements of its environment. However, containment creates a separate problem for Isoetes, which is that the gametophytes have no way to acquire energy on their own. Isoetes sporophytes solve this problem by provisioning starches and other nutrients to the spores as an energy reserve for the eventual gametophytes. [21] [22] Although not a homologous process, this provisioning is somewhat analogous to other modes of offspring resource investment in seed-plants, such as fruits and seeds. The extent to which resources provisioned to the megaspore also support the growth of the new sporophyte is unknown in Isoetes.

Dispersal

Spore dispersal occurs primarily in water (hydrochory) but may also occur via adherence to animals (zoochory) and as a result of ingestion (endozoochory). [15] [23] These are among the reasons suggested for the ornamentations of the spore, with some authors demonstrating that certain patterns seem well-adapted for sticking to relevant animals like waterfowl. [23] Another critical element of dispersal is the observation that in some species of Isoetes, the outer coat of megaspores have pockets that trap microspores, a condition known as synaptospory. [23] [24] Typically, heterospory means that colonization and long-dispersal are more difficult due to the fact that a single spore cannot grow a bisexual gametophyte and thus cannot establish a new population from a single spore as can happen in homosporous ferns. [25] Isoetes may mitigate this issue via microspores stuck to megaspores, greatly increasing the possibility of successful fertilization upon dispersal. [23] [24]

Taxonomy

Compared to other genera, Isoetes is poorly known. The first critical monograph on their taxonomy, written by Norma Etta Pfeiffer, was published in 1922 and remained a standard reference into the twenty-first century. [26] [27] Even after studies with cytology, scanning electron microscopy, and chromatography, species are difficult to identify and their phylogeny is disputed. Vegetative characteristics commonly used to distinguish other genera, such as leaf length, rigidity, color, or shape are variable and depend on the habitat. Most classification systems for Isoetes rely on spore characteristics, which make species identification nearly impossible without microscopy. [28]

Evolution

Undescribed Isoetites fossil Klondike Mountain Formation Isoetites sp UWBM37862 WaG 1996 img1.png
Undescribed Isoetites fossil
Klondike Mountain Formation

The earliest fossil that has been assigned to the genus is † Isoetes beestonii from the latest Permian [29] of New South Wales, Australia, around 252 million years ago. [30] However, the relationships of pre-Jurassic isoetaleans to modern Isotetes have been regarded as unclear by other authors. [3] Isoetites rolandii from the Late Jurassic of North America has been described as the "earliest clear example of a isoetalean lycopsid containing all the major features uniting modern Isoetes", including the loss of the elongated stem and vegetative leaves. Based on this, it has been stated that "the overall morphology of Isoetes appears to have persisted virtually unchanged since at least the Jurassic". [3] The timing of the origin of the crown group is uncertain. Wood et al (2020) asserted there to be no morphological features that define the major clades within Isoetes, and no fossils are known that can be definitively assigned to the crown group. [3] While Wood et al. suggested a young origin dating to the early Cenozoic based on molecular clock estimates [3] , the results were questioned by Wikström et al. (2023) who regarded the molecular clock as providing no firm evidence for the origin time of the genus, which could date to the Mesozoic or even the late Paleozoic, depending on the calibration method used. [4]

Extant species

As of November 2019, Plants of the World Online accepted the following extant species: [31]

Many species, such as the Louisiana quillwort and the mat-forming quillwort, are endangered species. Several species of Isoetes are commonly called Merlin's grass, especially I. lacustris , but also the endangered species I. tegetiformans .

Hybrids

Fossil species

Related Research Articles

<span class="mw-page-title-main">Gametophyte</span> Haploid stage in the life cycle of plants and algae

A gametophyte is one of the two alternating multicellular phases in the life cycles of plants and algae. It is a haploid multicellular organism that develops from a haploid spore that has one set of chromosomes. The gametophyte is the sexual phase in the life cycle of plants and algae. It develops sex organs that produce gametes, haploid sex cells that participate in fertilization to form a diploid zygote which has a double set of chromosomes. Cell division of the zygote results in a new diploid multicellular organism, the second stage in the life cycle known as the sporophyte. The sporophyte can produce haploid spores by meiosis that on germination produce a new generation of gametophytes.

<span class="mw-page-title-main">Spore</span> Unit of reproduction adapted for dispersal and survival in unfavorable conditions

In biology, a spore is a unit of sexual or asexual reproduction that may be adapted for dispersal and for survival, often for extended periods of time, in unfavourable conditions. Spores form part of the life cycles of many plants, algae, fungi and protozoa.

<span class="mw-page-title-main">Sporangium</span> Enclosure in which spores are formed

A sporangium, also known as a "sporange", is an enclosure in which spores are formed. It can be composed of a single cell or can be multicellular. Virtually all plants, fungi, and many other lineages form sporangia at some point in their life cycle. Sporangia can produce spores by mitosis, but in nearly all land plants and many fungi, sporangia are the site of meiosis and produce genetically distinct haploid spores.

<span class="mw-page-title-main">Alternation of generations</span> Reproductive cycle of plants and algae

Alternation of generations is the predominant type of life cycle in plants and algae. In plants both phases are multicellular: the haploid sexual phase – the gametophyte – alternates with a diploid asexual phase – the sporophyte.

<span class="mw-page-title-main">Lycopodiopsida</span> Class of vascular plants

Lycopodiopsida is a class of vascular plants known as lycopods, lycophytes or other terms including the component lyco-. Members of the class are also called clubmosses, firmosses, spikemosses and quillworts. They have dichotomously branching stems bearing simple leaves called microphylls and reproduce by means of spores borne in sporangia on the sides of the stems at the bases of the leaves. Although living species are small, during the Carboniferous, extinct tree-like forms (Lepidodendrales) formed huge forests that dominated the landscape and contributed to coal deposits.

<span class="mw-page-title-main">Sporophyte</span> Diploid multicellular stage in the life cycle of a plant or alga

A sporophyte is the diploid multicellular stage in the life cycle of a plant or alga which produces asexual spores. This stage alternates with a multicellular haploid gametophyte phase.

<span class="mw-page-title-main">Salviniales</span> Order of plants

The order Salviniales is an order of ferns in the class Polypodiopsida.

<i>Isoetes lacustris</i> Species of spore-bearing plant

Isoetes lacustris, the lake quillwort or Merlin's grass, is a boreal quillwort native on both sides of the northern Atlantic Ocean. Synonyms include Isoetes hieroglyphica.

<span class="mw-page-title-main">Microspore</span> Small land plant spores that develop into male gametophytes

Microspores are land plant spores that develop into male gametophytes, whereas megaspores develop into female gametophytes. The male gametophyte gives rise to sperm cells, which are used for fertilization of an egg cell to form a zygote. Megaspores are structures that are part of the alternation of generations in many seedless vascular cryptogams, all gymnosperms and all angiosperms. Plants with heterosporous life cycles using microspores and megaspores arose independently in several plant groups during the Devonian period. Microspores are haploid, and are produced from diploid microsporocytes by meiosis.

<span class="mw-page-title-main">Megaspore</span> Large spore in heterosporous plants that germinates into a female gametophyte

Megaspores, also called macrospores, are a type of spore that is present in heterosporous plants. These plants have two spore types, megaspores and microspores. Generally speaking, the megaspore, or large spore, germinates into a female gametophyte, which produces egg cells. These are fertilized by sperm produced by the male gametophyte developing from the microspore. Heterosporous plants include seed plants, water ferns (Salviniales), spikemosses (Selaginellaceae) and quillworts (Isoetaceae).

<i>Isoetes engelmannii</i> Species of plant in the family Isoetaceae

Isoetes engelmannii is a species of aquatic plant in the family Isoetaceae. It is referred to by the common names Engelmann's quillwort or Appalachian quillwort, and is the most widely distributed species of its genus in eastern North America. Its range extends from Ontario in the north, south to Florida and west Arkansas and Missouri. It can be found from April to October in temporary pools, bogs, marshes, stream edges, swamps and along wet roadsides.

Isoetes valida, commonly known as the strong quillwort or true quillwort, is an aquatic lycophyte native to eastern North America. It is found primarily in the Appalachian Mountains from Pennsylvania south to Alabama and Georgia. In addition, one collection of the plant was made in a railway ditch in Wilmington, Delaware in the 1860s, but this was most likely an accidental introduction.

<span class="mw-page-title-main">Heterospory</span> The production of spores of two different sizes and sexes by several groups of land plants

Heterospory is the production of spores of two different sizes and sexes by the sporophytes of land plants. The smaller of these, the microspore, is male and the larger megaspore is female. Heterospory evolved during the Devonian period from isospory independently in several plant groups: the clubmosses, the ferns including the arborescent horsetails, and progymnosperms. This occurred as part of the process of evolution of the timing of sex differentiation.

<i>Isoetes melanospora</i> Species of spore-bearing plant

Isoetes melanospora, commonly known as black-spored quillwort or black-spored Merlin's grass, is a rare and endangered aquatic lycophyte endemic to the U.S. states of Georgia and South Carolina. It grows exclusively in shallow, temporary pools on granite outcrops, often with only 2 cm of soil. 11 populations are known to exist in Georgia, while only one has been recorded in South Carolina, though this population is believed to be extirpated. The number of sites has dropped from 18 following its discovery due to habitat destruction caused by quarrying, trash dumping and trampling. New leaves quickly sprout after fall and winter rains, but during the dry summer months these typically shrivel.

Isoetes nuttallii, or Nuttall's quillwort, is a species of quillwort, a type of lycopod. It is native to shallow waters and other wet habitats of western North America from British Columbia to California. It produces up to 60 pointed, cylindrical, green to gray-green leaves, each 7 to 17 centimeters long. The velum completely covers the spherical sporangia, which are 5 millimeters long and 1.5 millimeters wide. The ligule is small and triangular. The megaspores are 400 to 500 micrometers in diameter. The microspores, which are spiny and covered in tubercles, are 28 to 31 micrometers long.

<i>Isoetes echinospora</i> Species of plant

Isoetes echinospora, also known as spiny quillwort, spiny-spored quillwort or spring quillwort is a species of quillwort in the Isoetaceae family, and is the most abundant species in Canada. It can be found in shallow aquatic environments from Labrador and Newfoundland to Alaska, and south to Pennsylvania, Wisconsin, Michigan, Colorado, and California. In Germany it is found in only two locations: the Feldsee and Lake Titisee, both in the High Black Forest.

Isoetes × eatonii, or Eaton's quillwort, is a hybrid between I. engelmannii and I. tenella. It can be found in ponds and slow moving rivers in Canada or in several New England states. In Canada, it has only been found in the Severn River in Ontario. In the United States, it has been found in Pennsylvania, New Jersey, and New York. It bears 12-100 long yellowish green leaves, each fine, soft, and 8 to 45 centimeters long. The unspotted tan colored sporangium are 12 millimeters long and 5 millimeters wide. The velum covers a sixth to a quarter of the sporangium. The elongated ligule is 3.5 millimeters long. The flattened white megaspores are 320 to 530 micrometers in diameter and bear short spiny ridges. The round microspores are 22 to 25 micrometers long.

<i>Isoetes riparia</i> Species of plant in the family Isoetaceae

Isoetes riparia, the shore quillwort, is a species of plant in the family Isoetaceae. It can be found in rivers, creeks, and tidal mud flats in southern Quebec and southeastern Ontario, south to eastern New York. It has 5 to 35 long, erect bright green to yellow-green leaves, which are 6 to 35 centimeters long. The velum covers one fourth of the sporangium, which can be 7 millimeters long and 4 millimeters wide. The elongated ligule can grow to be 3 millimeters long. The spherical megaspores are 430 to 680 micrometers in diameter with closely set ridges. The kidney-shaped microspores are 24-35 micrometers long, and usually have spine-tipped tubercules. The megaspores can sometimes come to resemble that of either I. echinospora, if the megaspores become eroded and bear projections that could resemble spines, or I. macrospora, if the broken ridges take a certain shape.

Isoetes macrospora, the big-spore quillwort, is a species of quillwort in the Isoetaceae family. It can be found in the deep water of low nutrient lakes in the Precambrian Shield as well as in Newfoundland, Nova Scotia, Quebec, and Ontario. In the United States, it has been found in Minnesota and south, through the Appalachian Mountains to Virginia. It bears 3 to 17 long, stiff dark green leaves, sometimes with recurving tips. The sporangium can be 5 millimeters long and 4 millimeters wide, covered from one sixth to one quarter by the velum. The triangular ligule can grow up to 2 millimeters long. The spherical, white megaspores are 400 to 800 micrometers in diameter, and bear ridges that form honeycomb-like areas. The kidney-shaped microspores are 32 to 50 micrometers long, each with evenly spaced smooth papillae.

<i>Isoetes tuckermanii</i> Species of plant in the family Isoetaceae

Isoetes tuckermanii, or Tuckerman's quillwort, is a tetraploid species of plant in the family Isoetaceae. It can be found in shallow water in Newfoundland, Nova Scotia, New Brunswick, and south through the New England states to Maryland. It bears 10 to 45 long bright green to yellow green leaves that are 4 to 25 centimeters long, usually erect, but sometimes recurved. The velum covers one fourth or less of the sporangium, which is usually unspotted, 5 millimeters long, and 3 millimeters wide. The white spherical megaspores are 400 to 650 micrometers in diameter, and bear rough-crested ridges that form a hexagonal honeycomb shape. The kidney shaped microspores are 24 to 33 micrometers long, bearing tubercles. It is very similar to I. macrospora, only reliably distinguishable by cytology or through careful megaspore measurement.

References

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  22. ↑ Abeli, Thomas; Mucciarelli, Marco (2010). "Notes on the Natural History and Reproductive Biology of Isoëtes malinverniana". American Fern Journal. 100 (4): 235–237. doi:10.1640/0002-8444-100.4.235. ISSN   0002-8444. JSTOR   41237871. S2CID   83658338.
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  32. ↑ Hassler, Michael & Schmitt, Bernd (November 2019). "Isoetes caroliniana". Checklist of Ferns and Lycophytes of the World. 8.11. Retrieved 18 November 2019.
  33. 1 2 3 Pigg, K.B. (2001). "Isoetalean lycopsid evolution: from the Devonian to the present". American Fern Journal. 91 (3): 99–114. doi:10.1640/0002-8444(2001)091[0099:ILEFTD]2.0.CO;2. S2CID   85852292.
  34. ↑ Hill, R.S. (1988). "Tertiary Isoetes from Tasmania". Alcheringa. 12 (2): 157–162. doi:10.1080/03115518808619003.
  35. ↑ Britton, D. M. (1993). "Isoëtes reticulata RS Hill 1987 (Alcheringa 12: 158) is an illegitimate name". American Fern Journal. 83 (4): 128. doi:10.2307/1547589. JSTOR   1547589.
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