Circumnutation of rice coleoptiles: its relationships with gravitropism and absence in lazy mutants

Abstract

Although circumnutation occurs widely in higher plants, its mechanism is little understood. The idea that circumnutation is based on gravitropism has long been investigated, but the reported results have been controversial. We used dark-grown coleoptiles of rice ( Oryza sativa L.) to re-investigate this issue. The following results supported the existence of a close relationship between gravitropism and circumnutation: (1) circumnutation disappears on a horizontal clinostat; (2) circumnutation is interrupted by a gravitropic response and re-initiated at a definable phase after gravitropic curvature; (3) circumnutation can be reestablished by submergence and a brief gravitropic stimulation in the coleoptiles that have stopped nutating in response to red light; and (4) lazy mutants show no circumnutation. In spite of these results, however, there were cases in which gravitropism and circumnutation could be separated. Firstly, the non-circumnutating lazy coleoptile showed nearly a wild-type level of gravitropic responsiveness in its upper half, although this part was an active site of both gravitropism and circumnutation in wild-type coleoptiles. Secondly, coleoptiles could nutate without overshooting the vertical when developing phototropic curvature. It is concluded that gravitropism influences, but it is not directly involved in the process of circumnutation. It is further suggested that a gravity signal, shared with gravitropism, contributes to the maintenance of circumnutation.

AtLAZY1 is a signaling component required for gravitropism of the Arabidopsis thaliana inflorescence

“…The atlazy1 and AtLAZY1‐RNAi lines also lacked the transient overshooting of the final angle displayed by the wild type (Figure d). Impaired hypocotyl gravitropism in the atlazy1 lines is similar to the lazy1 coleoptile gravitropism phenotype (Yoshihara and Iino, , ).…”

“…As rice LAZY1 was found to be essential for coleoptile circumnutation (Yoshihara and Iino, , ), a role for AtLAZY1 in circumnutation of hypocotyls and inflorescence stems was investigated. Hypocotyl circumnutation enhanced by treatment with the ethylene precursor, 1‐aminocyclopropane‐1‐carboxylic‐acid (ACC) (Binder et al ., ) was measured with the HYPO T race tool.…”

“…Moreover, analysis of agravitropic mutants pgm ‐ 1 ( phosphoglucomutase ‐ 1 ), sgr1 ( shoot gravitropism1 ) and sgr7 mutants revealed that gravitropism and circumnutation in Arabidopsis inflorescence stems share mechanistic components (Hatakeda et al ., ). In rice, coleoptile circumnutation was severely impaired by the lazy1 mutation (Yoshihara and Iino, ). Yet, AtLAZY1 was not found to play a strong role in the circumnutation of hypocotyls or inflorescence stems (Figure S5).…”

“…Pulvini of lazy1 mutants show a reduced gravitropic response (Abe and Suge, 1993). The lazy1 mutation also impairs gravitropism and circumnutation of rice seedling coleoptiles (Abe et al, 1994;Yoshihara and Iino, 2006).…”

LAZY Genes Mediate the Effects of Gravity on Auxin Gradients and Plant Architecture

“…Auxin gradients control the differential growth that sets the angle (Rosquete et al, 2013). Limiting the influence of gravity by growing plants in microgravity (Lyon, 1968;Hoson et al, 1999) or on a clinostat (Lyon, 1965;Lyon and Yokoyama, 1966;Yoshihara and Iino, 2006) produces the shapes and architectures that would develop if gravity-response mechanisms were not in operation. Some responses to gravistimulation given after a clinostat treatment are opposite to normal gravitropism, but nonetheless are controlled by auxin gradients (Lyon, 1972;Roychoudhry et al, 2013) established by PIN auxin efflux proteins (Rosquete et al, 2013).…”