The Developmental Cycle of Spirodela polyrhiza Turions: A Model for Turion-Based Duckweed Overwintering?

Abstract

Duckweeds are widely distributed small, simply constructed aquatic higher plants (the Lemnaceae) found on quiet freshwater surfaces. Species inhabiting temperate climates may have to cope with long periods of severe cold during the winter season. Several duckweeds form compact resting structures from the assimilatory fronds of the growing season that can bridge inhospitable conditions in a quiescent state. Of these, turions separate from the mother fronds and overwinter on the water body bottom in a dormant state. They can surface, germinate, and sprout to resume active growth upon warming in the spring. The turions of the largest duckweed, Spirodela polyrhiza, have been intensively examined as to ultrastructure, the factors governing their formation and release from dormancy, and the signals driving their germination and sprouting and the accompanying starch degradation. Comparative transcriptomics of assimilatory fronds and dormant turions are revealing the molecular features of this developmental cycle. The results illustrate an elegant sequence of reactions that ensures aquatic survival of even severe winters by frost avoidance in a vegetative mode. Since little is known about other duckweed resting fronds, the S. polyrhiza turion developmental cycle cannot be considered to be representative of duckweed resting fronds in general but can serve as a reference for corresponding investigations.

Keywords: Lemnaceae; Spirodela polyrhiza; dormancy; duckweeds; formation; germination; model organism; sprouting; turions.

Figure 1

The five genera of the Lemnaceae and their respective species, including the two interspecific hybrids Le. x japonica and Le. x mediterranea. Species reported to form resting fronds capable of growth that remain on the water surface as described in Section 2. are marked with blue, those reported to form resting fronds capable of growth that sink to the bottom of the water body are marked with yellow, and those reported to form true turions are marked with green. The images are of S. polyrhiza strain 9500, La punctata 5562, Le. minor 9441, Wa. gladiata 7173, and Wo. arrhiza 9528, all courtesy of Klaus Appenroth.

Figure 2

The life, or developmental, cycle of Spirodela polyrhiza. The main features of the cycle are designated in blue, and important principles governing these features, which are discussed further in the following Section 3.1, Section 3.2 and Section 3.3 are indicated in red. The images are of S. polyrhiza strain 9500, courtesy of Klaus Appenroth. Turions emerging from a colony of fronds are indicated by red arrows.

Figure 3

Features of S. polyrhiza turions that distinguish them from the vegetative fronds having given rise to them. Images are of S. polyrhiza strain 9500, courtesy of Klaus Appenroth. The red arrow points to a turion emerging from a mother frond.

Figure 4

The fate of the starch stored in dormant turions of S. polyrhiza. The breaking of turion dormancy during the winter upon after-ripening is accompanied by the release of small amounts of soluble short-chain carbohydrates from the starch that accumulate sufficiently to support germination of the non-dormant turion. When germination occurs upon warming in the spring, incident light transforms the red light-absorbing form of phytochrome (“Pr”) in the emerging shoot into the far red-absorbing form (“Pfr”) that initiates the phosphorylation of glucan, water dikinase (“GWD”) at the starch granule surface. Phosphorylated GWD transfers its phosphate group to the starch granule itself, which enables α-amylase to bind to the granule surface and initiate massive starch breakdown to release large amounts of soluble carbohydrates to support sprouting.