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Morphology of Zeylanidium lichenoides . (A) Phylogenetic relationship and schematic illustrations of the seedling body plan (upper) and the shoot system (lower) of Hypericaceae and Podostemaceae (modifi ed from Katayama et al., 2010 , 2011 ). Arrows indicate indeterminate shoots with a conventional shoot meristem; T-shaped lines indicate determinate shoots without a distinct shoot meristem. The red region implies cryptic embryonic shoot meristem, brown indicates the shoot, and green the leaf. (B) Side view of seedling at 20 days after sowing (DAS), with a reduced primary shoot with plumular leaves and no primary root. The arrowhead indicates the site where the adventitious root arises. (C) Top view of seedling at 30 DAS with plumular leaves. Adventitious root arising from a hypocotyl and forming adventitious leaves (root-borne shoots). (D) Adult plant growing in Kerala, India. Adventitious roots creeping on rock surface with root-borne shoots on lateral sides. al, adventitious leaf; ar, adventitious root; c, cotyledon; h, hypocotyl; pl, plumular leaf; pr, primary root, ps, primary shoot; rh, rhizoid; rs, root-borne shoot. Bars = 100 μm in B; 500 μm in C.
Source publication
Premise of the study:
The shoot apical meristem is the source of aerial shoot systems. In the aquatic eudicot family Podostemaceae, subfamily Podostemoideae, however, shoots develop in the absence of a distinct apical meristem. Previous studies suggest that the cryptic embryonic shoot meristem is involved in primary shoot development in some speci...
Citations
... The concept of "morphological misfits" is an eye-catcher that allows labelling of all kinds of morphological deviations in the wild, mainly based on major genetic changes such as homeosis (i.e., ectopic gene expression in a seemingly wrong position) and other kinds of developmental repatterning [36,79,80]. Morphological misfits are found in various aquatic vascular plants such as the duck-weeds (Lemna and allies in Araceae) [81] and the river-weeds (Podostemaceae) [22,[82][83][84], but also in terrestrial plants such as the gloxinia family (Gesneriaceae), containing one-leaf plants (members of the genera Monophyllaea and Streptocarpus) [69,85] and in plant groups containing both aquatic and terrestrial members such as the bladderworts (Utricularia, Lentibulariaceae) [22]. The bladderworts (genus Utricularia) belong-also with respect to molecular developmental genetics-to the best-known examples of morphological misfits in vascular plants. ...
... To do this, we need to look for, e.g., organ identity genes in order to define the structural categories clearly. For example, the KNOX/ARP module (as used by Katayama et al. [82,83], Cruz et al. [72,104]) helps with the identification of the leaf as a determinate unit, and the shoot as an indeterminate module in vascular plants. This approach seems to have promise in the cases where control genes for organ identity have been shown to exist, for example, Pax6, which is often accepted as the "master control gene" for eye development in arthropods and vertebrates [57,160]. ...
... When we cling to structural categories such as leaf, stem, and root for the description of the plant bodies in river-weeds, we get into trouble with either/or homology ("sameness") of the various plant parts. Then we are forced to accept the existence of structural intermediates such as "stem-leaf mixed organs" in Podostemaceae, as genetically analyzed by Katayama et al. [82,83]. This appellation is meant to indicate that these structures have some features of leaves, and some of stems, probably due to their unusual gene expression pattern and the lack of obvious SAMs [84]. ...
Plants and animals are both important for studies in evolutionary developmental biology (EvoDevo). Plant morphology as a valuable discipline of EvoDevo is set for a paradigm shift. Process thinking and the continuum approach in plant morphology allow us to perceive and interpret growing plants as combinations of developmental processes rather than as assemblages of structural units (“organs”) such as roots, stems, leaves, and flowers. These dynamic philosophical perspectives were already favored by botanists and philosophers such as Agnes Arber (1879–1960) and Rolf Sattler (*1936). The acceptance of growing plants as dynamic continua inspires EvoDevo scientists such as developmental geneticists and evolutionary biologists to move towards a more holistic understanding of plants in time and space. This review will appeal to many young scientists in the plant development research fields. It covers a wide range of relevant publications from the past to present.
... To reveal the evolutionary history of the "determinate shoot", Katayama et al. (2011Katayama et al. ( , 2013 performed embryological analyses of Zeylanidium tailichenoides, an Asian member, which was previously referred to as Z. lichenoides but was renamed by Kato and Koi (2018). During embryogenesis, a morphologically unrecognizable SAM, denoted as a cryptic SAM in Katayama et al. (2013), was observed accompanying the expression of STM ortholog (ZlSTM). ...
... To reveal the evolutionary history of the "determinate shoot", Katayama et al. (2011Katayama et al. ( , 2013 performed embryological analyses of Zeylanidium tailichenoides, an Asian member, which was previously referred to as Z. lichenoides but was renamed by Kato and Koi (2018). During embryogenesis, a morphologically unrecognizable SAM, denoted as a cryptic SAM in Katayama et al. (2013), was observed accompanying the expression of STM ortholog (ZlSTM). Following germination, ZlSTM expression is not maintained in the cryptic SAM and shifts to the adaxial base i.e., the axils of cotyledons, where the new determinate shoots arise. ...
... The synthesized RNA probes were partially hydrolyzed to ~ 300 bp with an alkaline solution (60 mmol L -1 Na 2 CO 3 and 40 mmol L -1 NaHCO 3 , pH 10.2) at 60 °C for 80 min. RNA in situ hybridization was conducted according to Katayama et al. (2013). ...
Shoots of the aquatic eudicot family, Podostemaceae, exhibit unusual organogenesis with mixed leaf and stem identities. New shoots arise at the base of the older shoot with shoot apical meristem (SAM) identity but the entire SAM differentiates into a “leaf” as it develops in the Podostemoideae subfamily. The “leaves” are tightly arranged in a zigzag manner to form an apparent distichous shoot as a whole. Although previous studies have suggested that Podostemoideae shoots have evolved by modifying the ancestral sympodial branching system in the basal Tristichoideae subfamily, this evolutionary scenario requires elucidation at the molecular level. To confirm that the shoots arise as axillary shoots, in the present study, we examined gene expression patterns in plumular shoots of Zeylanidium tailichenoides using CUP-SHAPED COTYLEDON 3 (CUC3) and SHOOT MERISTEMLESS (STM) orthologs, which are involved in the determination of axils and meristem formation in model plants. Expression of the CUC3 ortholog was detected at the adaxial base of cotyledons and parental shoots where the new shoots are initiated, while STM ortholog was expressed at the initiation site and in the young shoot primordia throughout early shoot development. The results demonstrate that each Z. tailichenoides shoot arises as an axillary bud in a manner similar to axillary meristem formation in model plants involving CUC3 and STM genes. Considering that each of the two cotyledons produces an axillary bud that in turn continues to form its own axillary bud independently, the apparent distichous shoot in Z.tailichenoides is not a single shoot, but a composite of two sympodially branched shoots.
... Zeylanidium lichenoides, like many other species of Podostemoideae, has a rudimentary primary shoot, which produces only a few leaves between the cotyledons. In an analysis of gene-expression pattern in the embryo and seedling, Katayama et al. (2013) showed that expression of an STM ortholog began in the apical part of the 16-celled embryo. By the heart-shaped embryo stage, its expression is restricted to the putative organizing center (OC) and the protodermal cells, forming a cryptic Katayama et al. (2010). ...
The moss-like river-weeds or Podostemaceae offer a special opportunity to study the diversity and evolution of plants that are adapted to extreme environments. This paper reviews multidisciplinary studies on this subject. Based on field work in the four continents, we discovered many species and several genera that are new components of biodiversity, and revealed the Podostemaceae floras of East Asia, Southeast Asia, and Australia. The historical biogeography of the family, i.e., the change in distribution in space and time, is characterized by a few dispersals between continents, followed by diversification within each continent. Local species may be derived from parts of separated populations of parental species, which consequently are paraphyletic. The remarkable morphological adaptations of Podostemaceae include the development of the horizontal axis in plant body, with which the plants adhere to rock surfaces under violent current. The vertical axis is reduced or lost and the horizontal axis develops in the embryo and seedling. We also found saltational organ-level variation, such as presence or absence of shoot, shoot apical meristem, root, and root cap; the form of shoot and root; the mode of root branching and leaf production; and the number of cotyledons. Morphological evolution may not be always adaptive to the habitats, which are rocks periodically submerged across the distribution range. Analyses of shoot regulatory gene expression found that, in contrast to the expression pattern in primitive species with ordinary shoots, which is comparable with Arabidopsis, the unique pattern in derived species may result in 'fuzzy' morphology of the shoot and leaf. Finally, problems for future study are pointed out.
... According to Japanese studies (e.g. Imaichi et al., 2005;Katayama et al., 2008Katayama et al., , 2010Katayama et al., , 2013Koi and Kato, 2010), the leaf primordium in vegetative shoots develops from the base of the opposing second youngest leaf primordium. The initiation of a new leaf primordium appears to be associated with degeneration of neighbouring cells, as shown by Imaichi et al. (2005), Koi et al. (2005), and Koi and Kato (2010) for Asian Podostemoideae. ...
... Developmental genes involved in bauplan deviations of Podostemoideae as compared with Tristichoideae Katayama et al. (2010Katayama et al. ( , 2013 investigated the mechanisms underlying shoot development in Podostemaceae by expression analysis of key developmental regulatory gene orthologues in model eudicots. STM (SHOOT MERISTEMLESS) and WUS are necessary for the formation and maintenance of the SAM in eudicots (including arabidopsis), and ARP (ASYMMETRIC LEAVES1/ROUGH SHEATH2/PHANTASTICA) promotes leaf identity (Gallois et al., 2002;Langdale and Harrison, 2008;Takeda and Aida, 2011). ...
... As a result, the leaves have 'a mixture of shoot and leaf, showing fuzzy morphology' (Kato, 2013, p. 45). According to the evolutionary model proposed by Katayama et al. (2010Katayama et al. ( , 2011Katayama et al. ( , 2013, the shoots in Podostemoideae grow by repetitive formation of stem-leaf mixed organs and this pattern is derived from the sympodial shoot branching of Tristichoideae and Weddellinoideae. The early loss of embryonic shoot and root meristems (i.e. ...
Background:
Various groups of flowering plants reveal profound ('saltational') changes of their bauplans (architectural rules) as compared with related taxa. These plants are known as morphological misfits that appear as rather large morphological deviations from the norm. Some of them emerged as morphological key innovations (perhaps 'hopeful monsters') that gave rise to new evolutionary lines of organisms, based on (major) genetic changes.
Scope:
This pictorial report places emphasis on released bauplans as typical for bladderworts (Utricularia, approx. 230 secies, Lentibulariaceae) and river-weeds (Podostemaceae, three subfamilies, approx. 54 genera, approx. 310 species). Bladderworts (Utricularia) are carnivorous, possessing sucking traps. They live as submerged aquatics (except for their flowers), as humid terrestrials or as epiphytes. Most Podostemaceae are restricted to rocks in tropical river-rapids and waterfalls. They survive as submerged haptophytes in these extreme habitats during the rainy season, emerging with their flowers afterwards. The recent scientific progress in developmental biology and evolutionary history of both Lentibulariaceae and Podostemaceae is summarized.
Conclusions:
Lentibulariaceae and Podostemaceae follow structural rules that are different from but related to those of more typical flowering plants. The roots, stems and leaves - as still distinguishable in related flowering plants - are blurred ('fuzzy'). However, both families have stable floral bauplans. The developmental switches to unusual vegetative morphologies facilitated rather than prevented the evolution of species diversity in both families. The lack of one-to-one correspondence between structural categories and gene expression may have arisen from the re-use of existing genetic resources in novel contexts. Understanding what developmental patterns are followed in Lentibulariaceae and Podostemaceae is a necessary prerequisite to discover the genetic alterations that led to the evolution of these atypical plants. Future molecular genetic work on morphological misfits such as bladderworts and river-weeds will provide insight into developmental and evolutionary aspects of more typical vascular plants.
... In the most derived forms, none of the conventional vegetative parts of angiosperms is recognizable and the whole takes a form more reminiscent of an alga than of a plant articulated into roots, stem, branches and leaves. Gene expression patterns studied by Katayama et al. (2010Katayama et al. ( , 2013 in two Podostemoideae reveal an indeterminate stem capped by something like a determinate "leaf", with new leaves/branches developing endogenously from the base of the "leaf". ...
Morphological misfits can be defined as a miscellaneous class of numerically marginal, often lately discovered taxa, deviating in one or more dramatic aspects from the structural organization of their closest relatives. Morphological misfits are a widely diverse set of taxa which according to their anatomical, ontogenetic and phylogenetic nature may offer the opportunity for a multiplicity of case studies in evolutionary developmental biology. Anatomically, there are modular misfits such as the paussinae beetles, with their extravagant antennae borne on a quite usual beetle body, and systemic misfits such as Wolffia among the flowering plants, reduced to a minute blob of green matter, and the also bloblike parasitic crustacean Sacculina among the animals. The former, but not the latter, are suggestive of developmental modularity. Ontogenetically, there are one-phase only misfits, such as blepharicerid midges (aberrant larvae but conventional midge-shaped adults), and whole-life-cycle misfits such as cycliophorans. The former, but not the latter, would suggest an evolutionary independence of developmental stages. Some misfits have diverged recently from their morphologically conservative closest relatives (e.g. the duckweeds (Lemnoideae) from conventional Araceae), while others, such as chaetognaths and Welwitschia, are the sole members of lineages which diverged very deeply in time from their closest known or putative relatives. The former, but not the latter, can provide obvious opportunities for investigating character evolvability.
