The ARG1-LIKE2 Gene of Arabidopsis Functions in a Gravity Signal Transduction Pathway That Is Genetically Distinct from the PGM Pathway

Abstract

The arl2 mutants of Arabidopsis display altered root and hypocotyl gravitropism, whereas their inflorescence stems are fully gravitropic. Interestingly, mutant roots respond like the wild type to phytohormones and an inhibitor of polar auxin transport. Also, their cap columella cells accumulate starch similarly to wild-type cells, and mutant hypocotyls display strong phototropic responses to lateral light stimulation. The ARL2 gene encodes a DnaJ-like protein similar to ARG1, another protein previously implicated in gravity signal transduction in Arabidopsis seedlings. ARL2 is expressed at low levels in all organs of seedlings and plants. arl2-1 arg1-2 double mutant roots display kinetics of gravitropism similar to those of single mutants. However, double mutants carrying both arl2-1 and pgm-1 (a mutation in the starch-biosynthetic gene PHOSPHOGLUCOMUTASE) at the homozygous state display a more pronounced root gravitropic defect than the single mutants. On the other hand, seedlings with a null mutation in ARL1, a paralog of ARG1 and ARL2, behave similarly to the wild type in gravitropism and other related assays. Taken together, the results suggest that ARG1 and ARL2 function in the same gravity signal transduction pathway in the hypocotyl and root of Arabidopsis seedlings, distinct from the pathway involving PGM.Gravity is one of the environmental cues that guides plant organs' growth. Most plant organs are characterized by a specific gravity set point angle, which defines their preferential growth vector relative to gravity (Firn and Digby, 1997). In young Arabidopsis seedlings, shoots grow upward, displaying negative gravitropism, whereas roots grow downward, toward the center of gravity (positive gravitropism; Bullen et al., 1990;Boonsirichai et al., 2002).Gravity perception by dicot organs involves primarily the sedimentation of amyloplasts within specialized cells (statocytes) located in the columella region of the root cap and in the starch sheath, which constitutes the endodermis of hypocotyls and inflorescence stems (Kiss et al., 1996;Kuznetsov and Hasenstein, 1996;Blancaflor et al., 1998; Weise et al., 2000). In shoots, sedimentable amyloplasts and the curvature response to gravistimulation occur along the elongation zone (for review, see Masson et al., 2002). After amyloplast sedimentation, signals are likely transduced within the endodermal cells, and physiological signals are transported laterally to affect elongation of cortical and epidermal cells. In roots, sites of gravity perception and curvature response may be physically separated (Poff and Martin, 1989). Hence, physiological signals resulting from activation of the gravity signal transduction pathway should be transported from the root cap columella to the elongation zones where the gravitropic curvature is initiated (for review, see Boonsirichai et al., 2002).Auxin is a physiological signal that has been shown to mediate the gravitropic response (for review, see Masson et al., 2002). In gravistimulated roots, auxin is redistributed asymmet...

ARL2, ARG1 and PIN3 define a gravity signal transduction pathway in root statocytes

“…The prominent localization of ARG1 and ectopically expressed ARL2 to the cell plate suggests that they are present in areas of high vesicle trafficking activity. Mutations in ARL2 or ARG1 do not affect the localization or expression of PIN2 ( Figure S2), and the mutants show normal growth responses to the auxin transport inhibitor 1-N-naphthylphthalamic acid (NPA) and unilateral light (Guan et al, 2003;Sedbrook et al, 1999). Therefore, if ARL2 and ARG1 function in PIN3 trafficking, they do so specifically within the gravity-signaling pathway.…”

“…The arg1-2 mutant lacks alkalinization of the columella cytoplasm and redistribution of auxin across the root tip following gravi-stimulation . arg1 and arl2 single mutants as well as arg1 arl2 double mutants show similar gravitropic defects, indicating that ARG1 and ARL2 function in the same gravity-signaling pathway (Guan et al, 2003). ARG1 and ARL2 each contain a J-domain near their N-termini, and a predicted coiled-coil motif near their C-termini (Guan et al, 2003;Sedbrook et al, 1999).…”

“…arg1 and arl2 mutants respond normally to auxin and auxin transport inhibitors and show normal phototropic bending, indicating that ARG1 and ARL2 function specifically in gravity sensing/signaling (Guan et al, 2003;Sedbrook et al, 1999). The arg1-2 mutant lacks alkalinization of the columella cytoplasm and redistribution of auxin across the root tip following gravi-stimulation .…”

“…arg1 and arl2 single mutants as well as arg1 arl2 double mutants show similar gravitropic defects, indicating that ARG1 and ARL2 function in the same gravity-signaling pathway (Guan et al, 2003). ARG1 and ARL2 each contain a J-domain near their N-termini, and a predicted coiled-coil motif near their C-termini (Guan et al, 2003;Sedbrook et al, 1999). J-domain proteins are present in organisms of all kingdoms, and make up a diverse gene family in Arabidopsis (Miernyk, 2001).…”

“…Mutations in two paralogous Arabidopsis genes, ARG1/ RHG1 and ARL2, result in slower kinetics of root and hypocotyl gravitropism (Fukaki et al, 1997;Guan et al, 2003;Sedbrook et al, 1999). arg1 and arl2 mutants respond normally to auxin and auxin transport inhibitors and show normal phototropic bending, indicating that ARG1 and ARL2 function specifically in gravity sensing/signaling (Guan et al, 2003;Sedbrook et al, 1999).…”