Photosynthetic sucrose acts as cotyledon-derived long-distance signal to control root growth during early seedling development in Arabidopsis

Abstract

The most hazardous span in the life of green plants is the period after germination when the developing seedling must reach the state of autotrophy before the nutrients stored in the seed are exhausted. The need for an economically optimized utilization of limited resources in this critical period is particularly obvious in species adopting the dispersal strategy of producing a large amount of tiny seeds. The model plant Arabidopsis thaliana belongs to this category. Arabidopsis seedlings promote root development only in the light. This response to light has long been recognized and recently discussed in terms of an organ-autonomous feature of photomorphogenesis directed by the red/blue light absorbing photoreceptors phytochrome and cryptochrome and mediated by hormones such as auxin and/or gibberellin. Here we show that the primary root of young Arabidopsis seedlings responds to an interorgan signal from the cotyledons and that phloem transport of photosynthesis-derived sugar into the root tip is necessary and sufficient for the regulation of root elongation growth by light.

Fig. 1.

Root growth in light and darkness 3–8 d after initiation of germination (daig). After 3 d in the light, seedlings were kept in continuous light (cL) or darkness (cD) and transferred from light to darkness (D) or darkness to light (L) after 4 and 5 daig as indicated.

Fig. 2.

Short-term kinetics of root growth (representative single measurements). (A) Intact light-grown seedlings were transferred to darkness 3 daig (D) and back to the light (broad field) 4 daig (L). (B) Perception of the light stimulus by the cotyledons. Light-grown seedlings were transferred to darkness 5 daig. At day 6 (L), a spotlight beam was directed to the whole shoot (1), a single cotyledon of an intact seedling (2), or the cotyledon of a seedling from which the other cotyledon + the shoot apex were dissected 5 daig (3). The dark control seedling (4) was growing next to the seedling of trace 1. (C) Selective irradiation of seedling parts. Intact seedlings grown as in B were partially irradiated with a spot light beam as outlined. In seedling 1, the visible leaf primordia at the shoot apex were dissected 5 daig. The distance between measuring points was 32 min.

Fig. 3.

Effect of cotyledon and apex amputation on root growth. After 5 daig in the light, the following seedling parts were dissected: visible leaf primordia (−apex), one cotyledon (−1 cot), entire apex and one cotyledon (−apex, 1 cot), two cotyledons (−2 cots), entire apex and two cotyledons (−apex, 2 cots). Root elongation was followed for further 3 d in the light. If present, the leaf primordia started to expand between day 1 and day 2 after amputation.

Fig. 4.

Effect of light on root elongation of mutants impaired either in the photomorphogenesis program (phyA,B/cry1,2) or the skotomorphogenesis program (cop1-4) grown in the absence (a) or presence (b) of 30 mM sucrose (suc). WT and mutant seedlings were kept either in darkness (D) or light (L) for 4 daig. Arrowheads indicate root tip.

Fig. 5.

Effect of photosynthesis inhibition on root and hypocotyl growth and its reversal by sucrose. Seedlings were grown for 4 daig in light (L) or darkness (D) with (gray bars) or without (white bars) 30 mM sucrose. (A) Without further treatment (control). (B) In a CO₂-depleted atmosphere (−CO₂). (C) With 0.1 μM norflurazone (San 9789) in the medium (20) (+NF). (D) Under far-red light (FR) with or without CO₂.

Fig. 6.

Root and hypocotyl growth in darkness as a function of sucrose concentration in the medium. Seedlings were grown for 4 daig on media containing 0–100 mM sucrose.

Fig. 7.

Effect of sucrose application to the root (A) or the cotyledons (B). Sucrose (0–1 M) or mannitol (0.1–1 M, osmotic control) were applied to the cotyledons or the root (above the growth zone) of seedlings grown for 5 daig in the light plus 1 d in darkness and subsequently kept in darkness for further 4 d.

Fig. 8.

Phenotypes of SUC2-deficient mutant seedlings grown in the absence (A and B) or presence (C) of sucrose. Seeds from the progeny of heterozygous SUC2/suc2 plants were germinated on medium without sucrose. After 4 daig in the light, seedlings differing from WT (10–12 mm root length) by having 1- to 2-mm-long roots (apparent homozygous individuals (A), were selected and kept on medium without (B) or with (C) 30 mM sucrose for further 4 d in the light.

Fig. 9.

Summarizing scheme to illustrate the dual role of light in early seedling development. After seed germination, seedlings follow the skotomorphogenic program of growth in darkness (1). Near the soil surface, incident light is perceived by phytochrome (Phy) and cryptochrome (Cry) photoreceptor systems (2) leading to onset of photomorphogenic development including establishment of the photosynthetic apparatus. In consequence, photosynthesis generates sugars (S) acting as interorgan signal and as fuel to drive root growth (3).