A leaf-derived signal is a quantitative determinant of floral form in Impatiens

Abstract

The completion of flower development in Impatiens balsamina requires continuous inductive (short-day) conditions. We have previously shown that a leaf-derived signal has a role in floral maintenance. The research described here analyzes the role of the leaf in flower development. Leaf removal treatments, in which plants were restricted to a specified number of leaves, resulted in flowers with increased petal number, up to double that of the undefoliated control. Similar petal number increases (as well as changes in bract number or morphology) were recorded when plants began their inductive treatment at a late developmental age or when plants of a nonreverting line (capable of floral maintenance in the absence of continuous short days) were transferred from short days to long days. Our data imply that the increased petal number was neither a response to stress effects associated with leaf removal nor a result of alterations in primordium initiation rates or substitutions of petals for stamens. Rather, the petal initiation phase was prolonged when the amounts of a leaf-derived signal were limiting. We conclude that a leaf-derived signal has a continuous and quantitative role in flower development and propose a temporal model for the action of organ identity genes in Impatiens. This work adds a new dimension to the prevailing ABC model of flower development and may provide an explanation for the wide variety and instabilities of floral form seen among certain species in nature.

Figure 1.

The Terminal Flower of Impatiens: SD (Control) and Leaf Removal Treatments from Day 0. (A) Terminal flower of red-flowered Impatiens grown in SD conditions. (B) Petal and petal-like organs of the terminal flower of Impatiens. From left to right in the top row are a sepal-like bract and partial petal (bract/sepal/petal tissue). In the middle row are a partial petal, a true petal, and a petal with white midvein. In the bottom row, staminate petals with only one petal lobe are shown. (C) to (E) Terminal flowers of plants from different treatments: (C) SD control; (D) SD-LR 1 cot treatment; and (E) SD-LR 2 cot treatment. Concentric circle diagrams to the right of each photograph show mean petal number and type and mean stamen number of flowers for each treatment. Distance between the circles is proportional to the number of petals of that type. The radius (from the center spot to the edge of the outermost circle) represents mean total number of petals and stamens for that treatment. Green denotes partial petals; red, true petals; orange, petals with white midveins; yellow, half petals with one petal lobe; and white, stamens. Means ±se are shown for each organ type. A central dot indicates carpels. Plant cartoons depict the experimental treatments (undefoliated, defoliated to one cotyledon, or defoliated to two cotyledons) giving rise to the terminal flower forms.

Figure 2.

Change in Mean Number of Leaves and Primordia over Time in SD and SD-LR 1 Cot Plants. These data were derived from plant dissections performed on days 0, 8, 14, 18, and 24. The points of initiation of the first true petal, petal with white midvein (WM), and stamen (deduced from mature plant dissections) are marked.

Figure 3.

The Terminal Flower of Impatiens: Day 8 Leaf Removal Treatments. The concentric circle diagrams show the mean petal number and type and mean stamen number for flowers of each day 8 treatment. (A) Plants defoliated to one cotyledon. (B) To two cotyledons. (C) To two cotyledons and one leaf. (D) To two cotyledons and two leaves. (E) To two cotyledons and three leaves. (F) The control treatment (induction in SD from day 0, no defoliation). Distance between the circles is proportional to the number of petals of that type. The radius (from the center spot to the outermost circle) represents the mean total number of petals and stamens in the treatment. Green denotes partial petals; red, true petals; orange, petals with white midveins; yellow, half petals with one petal lobe; white, stamens. Means ±se are shown for each organ type. Plant cartoons depict the experimental treatments giving rise to the terminal flower forms.

Figure 4.

Various Forms of the Terminal Flower of Red- and Purple-Flowered Impatiens Produced in Response to SD + LD, LD − SD, Leaf Removal Treatments, or Combinations of These. The diagrams show production of a hypothetical floral signal and its proposed quantitative relationship with organ identity under different treatments. (A) Undefoliated red-flowered plant in SD treatment. (B) Floral reversion of the red-flowered line, as described by Battey and Lyndon (1984) and Pouteau et al. (1997). (C) Leaf removal in red-flowered plants to restricted leaf number from day 8, as described in text. (D) Leaf removal in red-flowered plants to one cotyledon from day 0, as described in text. The effect of leaf removal on bract number is unclear, and this representation may therefore be an oversimplification. (E) Undefoliated purple-flowered plant in SD conditions. (F) Purple-flowered plants transferred to LD conditions after five SDs. Note that at the time of dissection, some plants in this treatment had produced stamens whereas others had not. (G) Red-flowered plants transferred to SD conditions after 14 LDs (from day 0). LD-SD treatment is described in text. (H) Reversion of the purple-flowered line as a result of leaf removal treatment, as described by Tooke et al. (1998). These plants are thought to be able to reflower after some time in LD conditions. A, B, and C indicate phases of meristem development associated with action of class A, B, and C genes (see Coen and Meyerowitz, 1991). Flower colors represent the red- and purple-flowered lines used.

Figure 5.

Temporal ABC Model of Flower Development in Impatiens. The model shows deduced timing of A, B, and C action in the development of the terminal flower of I. balsamina grown in SD conditions with no leaf removal (SD) and with leaf removal to only one cotyledon (SD 1 cot). This model is based on the rate of primordium initiation (determined by primordia counts of both treatments throughout the experiment) correlated with results of mature plant dissections (SD, n = 8; SD 1 cot, n = 9). Colored areas denote petal development. Partial petals have ⩾50% pigmentation; true petals have 100% petal pigmentation. A, B, and C are thought to overlap to specify staminate petals (white midveins/half petals).