Skip to main page content
Access keys NCBI Homepage MyNCBI Homepage Main Content Main Navigation
. 2020 Mar;257(2):371-390.
doi: 10.1007/s00709-019-01443-6. Epub 2019 Oct 28.

Unusual Developmental Morphology and Anatomy of Vegetative Organs in Utricularia Dichotoma-Leaf, Shoot and Root Dynamics

Affiliations
Free PMC article

Unusual Developmental Morphology and Anatomy of Vegetative Organs in Utricularia Dichotoma-Leaf, Shoot and Root Dynamics

Markus S Reut et al. Protoplasma. .
Free PMC article

Abstract

The terrestrial carnivorous species Utricularia dichotoma is known for a great phenotypic plasticity and unusual vegetative organs. Our investigation on 22 sources/populations revealed that after initiation of a leaf and two bladders on a stolon, a bud was formed in the proximal axil of the leaf, developing into a rosette with up to seven organs. The first two primordia of the bud grew into almost every possible combination of organs, but often into two anchor stolons. The patterns were generally not population specific. The interchangeability of organs increased with increasing rank in the succession of organs on stolon nodes. A high potential of switching developmental programs may be successful in a fluctuating environment. In this respect, we were able to show that bladders developed from anchor stolons experimentally when raising the water table. Anatomical structures were simple, lacunate and largely homogenous throughout all organs. They showed similarities with many hydrophytes, reflecting the plant's adaptation to (temporarily) submerged conditions. The principal component analysis was used in the context of dynamic morphology to illustrate correlations between organ types in the morphospace of U. dichotoma, revealing an organ specific patchwork of developmental processes for typical leaves and shoots, and less pronounced for a typical root. The concept and methods we applied may prove beneficial for future studies on the evolution of Lentibulariaceae, and on developmental morphology and genetics of unusual structures in plants.

Keywords: Bladderworts; Dynamic morphology; Pleiochasia; Polypompholyx; Utricularia; Utricularia dichotoma.

Conflict of interest statement

The authors declare that they have no conflict of interest.

Figures

Fig. 1
Fig. 1
Early development of organs on stolons of U. dichotoma. a Stolon tip on a plant from Strathgordon, Tasmania, with the first foliage leaf (L1) and two flanking bladders (b2–b3) arising nearly simultaneously and initiating a stolon node. b Stolon tip on a cultivated plant from New Zealand showing the first leaf (L1) growing faster than the bladders (b2–b3). c Stolon tip on a plant from Bog Inn, Pureora Forest, New Zealand, with the bladders (b2–b3) growing faster than the first leaf (L1); primordia 4 and 5 are barely visible; a new bladder primordium develops on the next node at the stolon tip. d Simple stolon (s) of U. dichotoma from Anglesea, Victoria, Australia, with a juvenile bladder (b1) and a bladder primordium (b2) close to the stolon tip (star). e Stolon of the cultivated ‘robust clone’ from Newcastle, NSW, Australia, showing a node with a leaf (L1) and two flanking bladders (b2–b3); a rosette with primordia of two anchor stolons (a4–a5) and three additional primordia (arrows) develops in central and proximal position at the leaf base (same tip as in Fig. 2d). Numbers of organs/primordia represent the rank in the developmental sequence. Scale bar is 0.1 mm in ac and 0.3 mm in de
Fig. 2
Fig. 2
Further development of organs on stolon nodes, and elongation of stolons of U. dichotoma. a Stolon node of a plant from Bog Inn, Pureora Forest, New Zealand, showing the common pattern with a first foliage leaf (L1), two juvenile bladders (b2–b3), and a rosette with two anchor stolons (a4–a5) and a primordium (5) of unknown developmental fate. b Stolon node of a plant from the Kopouatai Peat Dome, New Zealand, showing the first leaf (L1) and three bladders (b2, b3 and b4), an anchor stolon (a5), and two primordia (p). c Runner stolon (R) of a plant from Lake Ohia, New Zealand, with two bladders (b2–b3) and a rosette of organs terminating with an inflorescence (star). The first foliage leaf is missing or was detached; other organs cannot be determined. d Cultivated ‘robust clone’ from Newcastle, NSW, Australia, showing the succession of nodes I–III along the elongating stolon. A close-up of nodes II and III is shown in Fig. 1e. Numbers of organs/primordia represent the rank in the developmental sequence. The arrows point to the direction of the stolon tip. Scale bar is 0.3 mm
Fig. 3
Fig. 3
Organotaxis of rosettes on stolon nodes of U. dichotoma ‘Chestnut’ from Victoria, Australia (a), and of U. dichotoma from Strathgordon, Tasmania (bd). Initiation of stolon nodes of ad is with a first foliage leaf (L1) and two bladders (b2–b3). a Rosette of two anchor stolons and three primordia (6–8). b Rosette of an anchor stolon (a4), a leaf (L5) and five primordia (6–10). c Rosette of four primordia (4–7). d Rosette of two leaves (L1 = removed, L4), a runner stolon (R5), and four primordia (r) in decentralized position at the leaf base. Numbers of organs/primordia represent the rank in the developmental sequence. Scale bar is 0.3 mm for a, 0.1 mm for b and 0.2 mm for cd
Fig. 4
Fig. 4
Generalized pattern of stolon branching in U. dichotoma. On the upper sector of the runner stolon (R; green = upper/adaxial sector, blue = lower/abaxial sector), after the development of a first foliage leaf (L) and two bladders (b), organs grow from the base of the leaf in a rosette (r). a(s)/x = develops into an anchor stolon (a) which may turn into a simple stolon (s) or develops (less often) into another organ type (x) such as a bladder, a leaf, or a runner stolon at the same insertion. Primordia (p; organ rank 6 or higher) develop into a, s, b, L, or R. I = inflorescence (red)
Fig. 5
Fig. 5
Most abundant patterns of organ combinations in position 4 and 5 of rosettes on a runner stolon node in U. dichotoma. After development of a first foliage leaf (L1) and two bladders (b2-b3), a rosette with next primordia (4–5) was built at the base of the leaf. The first organ of the rosette was either an anchor stolon (a4), a bladder (b4), a leaf (L4), or a runner stolon (R4). The sequence continues with the development of an anchor stolon (a5), a bladder (b5), a leaf (L5), or a runner stolon (R5). During further elongation, anchor stolons may build bladders; in this form, they are called ‘simple stolons’ (s). Numbers of organs/primordia represent the rank in the developmental sequence. Organs of ranks 4 and 5 may be inverted. Populations/sources (cf. Table 1 for abbreviations), in which the organ combinations of rank 4–5 were found, are shown in boxes in italic, whereas, e.g. ‘all -Oh, -La, etc.’ means that this combination was found in all populations except for the material from Lake Ohio (Oh), Lake Pearson (La), etc. Note that there may be more sources shown for a specific organ in rank 4 than sources for rank 4 and 5 in sum, since they may have contained nodes with unidentifiable organs after position 4
Fig. 6
Fig. 6
Anatomy of the stolon tip and the leaf of U. dichotoma. a Longitudinal view through a stolon of U. dichotoma from Katoomba, NSW, Australia, showing photosynthetically active tissue below the epidermis (ep) of the foliage leaf (L) and on the upper side of the runner stolon (R). One vascular strand (v) is visible within the runner stolon. bd Cross sections through foliage leaves. b Plant from Newcastle, NSW, Australia, with an epidermis (ep) on the upper and lower side of the leaf, spongy parenchyma (sp), and a vascular strand (v). Details of the vascular tissue (in the rectangle) are outlined in d. c Plant from New Zealand with spongy parenchyma (sp) and one vascular strand consisting of one tracheary xylem element (x). The epidermal cells (ep) of the upper side of the leaf are more irregular in shape than the ones of the lower side. The irregular shape of the cells of the upper leaf epidermis is probably caused by tissue shrinkage prior or during the fixation process of the specimen. d Details of the vascular strand of picture b showing one tracheary xylem element (x) and at least two distinctive phloem tissues (ph). In leaves of b and c chloroplasts are more abundant in parenchyma cells of the upper leaf side. Scale bar is 0.1 mm in ac and 0.02 mm in d
Fig. 7
Fig. 7
Cross sections through stolons and bladder stalks of U. dichotoma with spongy parenchyma (sp), aerenchyma (ae) and tracheary xylem elements (x). a Anchor stolon of a plant from New Zealand. b Apical region of an anchor stolon of the alpine form from Falls Creek, Victoria, Australia. c Trap stalk of a plant from New Zealand. d Close-up of a trap stalk of a plant from Newcastle, NSW, Australia. e Runner stolon of a plant from Newcastle, NSW, Australia. The vascular bundle is completely surrounded by parenchyma cells, visualized by the red borderline. Details are shown in Fig. 8d. Scale bar is 0.02 mm in ad and 0.05 mm in e
Fig. 8
Fig. 8
Glandular and vascular tissue of runner stolons of U. dichotoma from Newcastle, NSW, Australia (a, b, d, e) and New Zealand (c). a, b Glandular (button-like) trichomes, more or less sunken in the epidermis. ce Vascular bundles with xylem element (x) and phloem groups (ph). c Tissues look irregular or squeezed, and phloem elements are difficult to identify. d Detail from Fig. 7e showing one xylem element and four phloem groups. e Vascular bundle with one xylem element (x) and four phloem groups (ph). The arrow points to a sieve plate. Scale bar is 0.02 mm
Fig. 9
Fig. 9
Principal component analysis of modalities (developmental processes) of vegetative organs of U. dichotoma, the root of P. moranensis, and a selection of typical roots, shoots and leaves. Principal component 1 (x-axis) is 37.34%; principal component 2 (y-axis) is 19.60%. a Morphospace of organs included in the PCA showing their distribution and distances (correlation) to each other (cf. Table 4 for abbreviations). Typical shoots and leaves are grouped (SR = SR1–4, SC = SC1–4, SD = SD1–4, LC = LC1–8, LE = LE1–4), and confidence ellipses (CI = 95%) of the groups are shown. b Distance biplot showing the distribution of organs in relation to modalities used in the PCA (see Table 3 for numbers of modalities and their meaning). Adjacent modalities show a positive correlation; opposite modalities indicate a negative correlation. Organs close to a modality axis are strongly influenced by the respective modality. A longer modality axis indicates that the modality has contributed more to the PCA.

Similar articles

See all similar articles

Cited by 1 article

References

    1. Adlassnig W, Peroutka M, Lambers H, Lichtscheidl IK. The roots of carnivorous plants. Plant Soil. 2005;274:127–140.
    1. Arber A. Water plants. A study of aquatic angiosperms. Cambridge: Cambridge University Press; 1920.
    1. Arber A. The natural philosophy of plant form. Cambridge: Cambridge University Press; 1950.
    1. Barta J, Stone JD, Pech J, Sirová D, Adamec L, Campbell MA, Štorchová H. The transcriptome of Utricularia vulgaris, a rootless plant with minimalist genome, reveals extreme alternative splicing and only moderate sequence similarity with Utricularia gibba. BMC Plant Biol. 2015;15:78–14. doi: 10.1186/s12870-015-0467-8. - DOI - PMC - PubMed
    1. Brugger J, Rutishauser R. Bau und Entwicklung landbewohnender Utricularia-Arten. Bot Helv. 1989;99:91–146.

LinkOut - more resources

Feedback