MAX4andRMS1are orthologous dioxygenase-like genes that regulate shoot branching inArabidopsisand pea

Abstract

Shoot branching is inhibited by auxin transported down the stem from the shoot apex. Auxin does not accumulate in inhibited buds and so must act indirectly. We show that mutations in the MAX4 gene of Arabidopsis result in increased and auxin-resistant bud growth. Increased branching in max4 shoots is restored to wild type by grafting to wild-type rootstocks, suggesting that MAX4 is required to produce a mobile branch-inhibiting signal, acting downstream of auxin. A similar role has been proposed for the pea gene, RMS1. Accordingly, MAX4 and RMS1 were found to encode orthologous, auxin-inducible members of the polyene dioxygenase family.Supplemental material is available at http://www.genesdev. org.Received December 6, 2002; revised version accepted March 20, 2003. Variation in shoot branching is an important cause of diversity in plant form. Individual species have a characteristic branching pattern, which can change through the life cycle in response to developmental cues and to environmental conditions (Cline 1991;Beveridge et al. 2003). Branching control therefore requires the integration of many signals, both known and unknown.Shoot branches arise from axillary meristems that form in the axils of leaves on the primary shoot axis. The axillary meristems themselves initiate leaves to form a bud. Bud growth can arrest but has the potential to reactivate to produce a shoot branch. Removal of the primary shoot apex results in activation of arrested axillary buds. The ability of the shoot apex to repress axillary bud growth is termed apical dominance. Thimann and Skoog (1933) reported that a compound, derived from the shoot apex, and later identified as auxin (indole-3-acetic acid), could inhibit the growth of lateral buds when applied to the stump of a decapitated plant. Subsequent work has provided multiple lines of evidence in support of auxinmediated bud inhibition in planta. However, a second messenger must relay the auxin signal into the bud because apically derived auxin is not transported into buds (Morris 1977) and exogenous auxin applied directly to buds does not inhibit their growth (Cline 1996).One model proposes that the effect of auxin on bud growth is mediated by cytokinin. Cytokinin can directly promote bud growth (Cline 1991); transgenic plants with increased auxin levels have reduced cytokinin levels (Eklö f et al. 2000), and cytokinin export from roots increases after decapitation, with this increase being abolished by application of auxin to the decapitated stump (Bangerth 1994). However, there is also good evidence for novel regulators of bud growth downstream of auxin. The ramosus mutants (rms1 to rms5) of pea (for reviews, see Beveridge 2000; Beveridge et al. 2003) have increased lateral branching, but this phenotype can be almost completely rescued by grafting a wild-type (WT) rootstock to an rms1, rms2, or rms5 mutant scion. Such grafting studies show that RMS1 and RMS5 are required for the production of a graft transmissible signal that moves from root to shoot and inhibits branching ...

Strigolactone Acts Downstream of Auxin to Regulate Bud Outgrowth in Pea and Arabidopsis

“…Previous studies have shown that auxin positively regulates SMS synthesis gene expression (Sorefan et al, 2003;Bainbridge et al, 2005;Foo et al, 2005;Johnson et al, 2006;Arite et al, 2007), also suggesting that strigolactones could function downstream of auxin to inhibit bud outgrowth. Auxin regulation of the expression of the SMS synthesis gene CCD8 was demonstrated to be AXR1 dependent in Arabidopsis (Bainbridge et al, 2005).…”

“…Auxin has been shown to promote the expression of SMS synthesis genes (Sorefan et al, 2003;Bainbridge et al, 2005;Foo et al, 2005;Johnson et al, 2006;Arite et al, 2007). As a result, branching mutants defective in auxin response may have reduced strigolactone biosynthesis, which may be the cause of their increased branching phenotype.…”

“…Decapitation resulted in reduced IAA levels and decreased expression of SMS synthesis genes (Sorefan et al, 2003;Foo et al, 2005;Johnson et al, 2006). Applying IAA to the decapitated plants rescued the drop in gene expression (Sorefan et al, 2003;Foo et al, 2005;Johnson et al, 2006).…”

“…Breakthroughs in cloning revealed that rms1, max4, dad1, and d10 SMS synthesis mutant phenotypes were caused by mutations in an orthologous gene, CAROT-ENOID CLEAVAGE DIOXYGENASE8 (CCD8; Sorefan et al, 2003;Snowden et al, 2005;Arite et al, 2007). Likewise, RMS5, MAX3, and D17/HTD1 were found to encode CCD7 (Booker et al, 2004;Johnson et al, 2006;Zou et al, 2006).…”

“…Auxin is known to promote the expression of SMS synthesis genes (Sorefan et al, 2003;Bainbridge et al, 2005;Foo et al, 2005;Johnson et al, 2006;Arite et al, 2007). Decapitation resulted in reduced IAA levels and decreased expression of SMS synthesis genes (Sorefan et al, 2003;Foo et al, 2005;Johnson et al, 2006).…”