Chemistry and biology of phototropism‐regulating substances in higher plants

Abstract

Most people are familiar with the sight of a young seedling bending towards a window or the brightest source of light to which it is exposed. This directional growth response is known as phototropism, which is caused by a lateral growth-promoting auxin in the bending organ (Cholodny-Went theory, cited in high school textbook). Recently, however, Bruinsma et al., Weiler et al., and Hasegawa et al. independently found that the shaded half did not contain more auxin than the illuminated one. Instead it was found that the even distribution of auxin was accompanied by a lateral gradient of growth inhibiting substances during phototropic curvature (Bruinsma-Hasegawa theory). We have isolated some photo-induced growth inhibitory substances related to phototropism, benzoxazolinones from light-grown maize shoots (Zea mays L.), raphanusanins from radish hypocotyl (Raphanus sativus var. hortensis f. gigantissimus M.), indolyacetonitrile from light-grown shoots (Brassica oleacea L.), 8-epixanthatin from sunflower hypocotyl (Helianthus annus L.), and quite recently uridine from oat coleoptile (Avena sativa L.). Chemical analyses have shown phototropic stimulations to cause curvature by inducing a local unequal distribution of growth-inhibiting substances that antagonize auxin in its cell-elongating activity. Finally, a model is presented for further studies on phototropism.

Induction of ß-glucosidase activity in maize coleoptiles by blue light illumination

“…In contrast to these reports, however, Iino (1991) reported the existence of a lateral gradient in endogenous IAA during phototropism in maize coleoptiles by use of the indolo-apyrone method, supporting the Cholodny-Went theory. However, the spectrometric assay has a shortcoming: high instability of the indolo-a-pyrone derivative causes poor reproducible of measurements, and the specificity of the method may be equivocal (Pickard 1985;Yamamura and Hasegawa, 2001). On the other hand, evidence showing that phototropism is caused by blue light-induced local accumulation of growth inhibitor(s) in the presence of an unchanged, even distribution of auxin, has been presented (Bruinsma et al, 1975;Franssen and Bruinsma, 1981;Hasegawa et al, 1989;Bruinsma and Hasegawa, 1990;Togo and Hasegawa, 1991;Hasegawa and Yamada, 1992;YokotaniTomita et al, 1999;Hasegawa et al, 2001;Yamamura and Hasegawa, 2001;Yamada et al, 2003;Hasegawa et al, 2004a, b;Tamimi, 2004) and constituted the basis of the Bruinsma-Hasegawa theory.…”

“…However, the spectrometric assay has a shortcoming: high instability of the indolo-a-pyrone derivative causes poor reproducible of measurements, and the specificity of the method may be equivocal (Pickard 1985;Yamamura and Hasegawa, 2001). On the other hand, evidence showing that phototropism is caused by blue light-induced local accumulation of growth inhibitor(s) in the presence of an unchanged, even distribution of auxin, has been presented (Bruinsma et al, 1975;Franssen and Bruinsma, 1981;Hasegawa et al, 1989;Bruinsma and Hasegawa, 1990;Togo and Hasegawa, 1991;Hasegawa and Yamada, 1992;YokotaniTomita et al, 1999;Hasegawa et al, 2001;Yamamura and Hasegawa, 2001;Yamada et al, 2003;Hasegawa et al, 2004a, b;Tamimi, 2004) and constituted the basis of the Bruinsma-Hasegawa theory. As candidates for growth inhibitory substances involved in phototropism, 4-methylthio-3-butenyl isothiocyanate and raphanusanins in radish hypocotyls (Hasegawa et al, 2000), uridine in oat coleoptiles , 8-epixanthatin in sunflower hypocotyls (Yokotani-Tomita et al, 1997), 4-hydroxy-2,3-dimethyl-2-nonen-4-olide from cress (Lepidium sativum) seedlings (Hasegawa et al, 2002), indole-3-acetonitrile from Arabidopsis hypocotyls (Hasegawa et al, 2004a) and 2,4-dihydroxy-7-methoxy-1,4-benzoxazin-3-one (DIM-BOA) and 6-methoxy-benzoxazolinone (MBOA) from maize coleoptiles Anai et al, 1996;Hasegawa et al, 2004b) have been isolated and identified.…”

Isolation and identification of blue light-induced growth inhibitor from light-grown Arabidopsis shoots

“…Cabbage that accumulates 3-indolylmethyl-glucosinolate also contains myrosinase, which is activated by phototropic stimulation to convert 3-indolylmethyl-glucosinolate into IAN. The resulting increase of IAN inhibits auxin-induced growth of cabbage hypocotyls (Yamamura and Hasegawa 2001). In the present study, IAN inhibited the hypocotyl growth of the nph3-101 mutant as well as that of the wild-type, suggesting that the nph3-101 mutant may be deficient in the IAN biosynthetic pathway after activation of the phototropic receptor(s).…”

“…However, the results of the present study are in full agreement with the general conclusion from all our experiments on phototropism in higher plants hitherto, viz. that this phenomenon is regulated by the lateral gradient of illumination-induced inhibitor(s) of elongation growth, independent of redistribution of IAA (Bruinsma and Hasegawa 1990;Yamamura and Hasegawa 2001).…”

“…From recent molecular genetic studies using phototropism mutants of Arabidopsis thaliana, it has been generally held up that unilateral blue light is absorbed into the photoreceptors phototropins (and cryptochromes), which activates the signaling pathways and induces the uneven distribution of regulator(s) of phototropic growth responses, resulting in phototropic curvature (Liscum and Briggs 1995;Ahmad et al 1998;Sakai et al 2000;Briggs et al 2001). Wherever those regulators have been identified it turned out that not the auxin, IAA, but rather growth-inhibitory substances were involved (Bruinsma and Hasegawa 1990;Yamamura and Hasegawa 2001).…”