Similarities and differences between phytochrome-mediated growth inhibition of coleoptiles and seminal roots in rice seedlings

In rice, light is known to inhibit the growth of coleoptiles and seminal roots of seedlings through phytochrome. Here we investigated the light-induced growth inhibition of seminal roots and compared the results with those recently determined for coleoptiles. Although three rice phytochromes, phyA, phyB and phyC functioned in a similar manner in coleoptile and seminal root, the Bunsen-Roscoe law of reciprocity was not observed in the growth inhibition of seminal root. We also found coiling of the seminal root at the root tip which appeared to be associated with the photoinhibition of seminal root growth. This could be a new light-induced phenomenon in certain cultivars of rice.Key words: growth, hypocotyl, Oryza sativa, phytochrome, seminal rootPhytochrome-mediated growth inhibition was reported for both coleoptiles and seminal roots of rice seedlings in the same year by two research groups in Nagoya and Tohoku University in Japan, respectively.^1,2 Forty years after the findings, a detailed photobiological study was carried out for the coleoptile growth inhibition.³ In this study, we examined photoinhibition of seminal root growth, and found similarities and differences between light-induced growth inhibition of the two organs in rice seedlings. Although coleoptile growth was inhibited by pulses of light, growth inhibition of seminal roots required light irradiation longer than 6 h. The Bunsen-Roscoe law of reciprocity was not observed in the growth inhibition of seminal root. Action spectra were determined for the growth inhibition of coleoptiles, and the mode of inhibition was found to depend on the age of the coleoptiles. At the early stage of development [40 h after inducing germination (AIG)], photoinhibition was predominantly due to the phyB-mediated low-fluence response (LFR), but at the late developmental stage (80 h AIG), it consisted of the phyA-mediated very low-fluence response (VLFR) as well as the phyB-mediated LFR.^3,4 In the case of root growth, the sensitivity of photoinhibition also depended on age, and was most sensitive in the period of 48–96 h AIG when seedlings were irradiated for 24 h. Using rice phytochrome mutants,⁵ we found that far-red light for root growth inhibition was perceived exclusively by phyA, that red light was perceived by both phyA and phyB, and that phyC had little or no role in growth inhibition. Furthermore, the fluence rate required for phyB-mediated inhibition was more than 10,000-fold greater than that required for phyA-mediated inhibition. These characteristics of photoinhibition in seminal roots are similar to those found in coleoptiles at the late stage of development.³ In seminal roots, photoinhibition appeared to be mediated by photoreceptors in the root itself.Interestingly, coiling of the root tips always occurred when root growth was inhibited under the light condition (Fig. 1B). Under continuous light irradiation, rice seeds germinated ∼30 h AIG. Seminal roots formed a coil at the root tips during the 48–96 h period AIG, and stopped growing. When they were irradiated for only 24 h on the 3rd day AIG, coils started to form just after the end of irradiation. The roots continued to coil for ∼28 h and then began growing straight again (Fig. 1C). The coils were larger and looser than those formed under continuous light condition (Fig. 1, Open in a separate windowFigure 1Light irradiation induces coiling of root tips in rice seedlings (Oryza sativa cv. Nipponbare). A rice seedling was grown in the dark (A), or in continuous white light (55 µole m⁻² s⁻¹) (B) for 7 d at 28°C. In (C), it was irradiated by white light for 24 h during the 48–72 h period after inducing germination, and kept in the dark again until the 7th day. Arrows and arrowheads indicate the seminal and crown roots, respectively. Seedlings were grown in glass tubes of 3-cm diameter.

Table 1

The size of coil of root tips formed after white light irradiation

Light irradiation	Diameter* (mm)	Length* (mm)	Number of turns*
Continuous irradiation for 7 d	1.96 ± 0.41	2.70 ± 0.63	4.6 ± 0.8
24 h-long irradiation during the 48–72 h period after inducing germination	2.60 ± 0.44	3.33 ± 0.19	2.3 ± 0.5

Open in a separate window* Mean and SD of 4-7 seedlings.We also found that light exposure had an opposite effect on the growth of the seminal and crown roots of rice seedlings. Light inhibited the growth of seminal roots, whereas it promoted the growth of crown roots. In fact, light was found to promote growth of Arabidopsis primary roots, in which phyA and phyB were found to be responsible for photoperception as well as photosynthetic activity.⁶ In rice seedlings, growth orientation of the crown roots is also affected by light exposure, whereas growth orientation of the seminal roots is controlled solely by the gravity vector. The crown roots grow in a horizontal direction in the dark, while they grow toward the gravity vector in the light.⁷ The contrasting responses to light in the seminal and crown roots are likely to help the transition of rice seedlings from the embryonic root system, in which the seminal roots are predominant, to the fibrous root system, which contains numerous crown roots.