The hpa1 Mutant of Arabidopsis Reveals a Crucial Role of Histidine Homeostasis in Root Meristem Maintenance

Abstract

Histidine (His) is an essential ingredient for protein synthesis and is required by all living organisms. In higher plants, although there is considerable evidence that His is essential for plant growth and survival, there is very little information as to whether it plays any specific role in plant development. Here, we present evidence for such a role of this amino acid in root development in Arabidopsis (Arabidopsis thaliana) from the characterization of a novel Arabidopsis mutant, hpa1, which has a very short root system and carries a mutation in one of the two Arabidopsis histidinol-phosphate aminotransferase (HPA) genes, AtHPA1. We have established that AtHPA1 encodes a functional HPA and that its complete knockout is embryo lethal. Biochemical analysis shows that the mutation in hpa1 only resulted in a 30% reduction in free His content and had no significant impact on the total His content. It did not cause any known symptoms of His starvation. However, the mutant displayed a specific developmental defect in root meristem maintenance and was unable to sustain primary root growth 2 d after germination. We have demonstrated that the root meristem failure in the mutant is tightly linked to the reduction in free His content and could be rescued by either exogenous His supplementation or AtHPA1 overexpression. Our results therefore reveal an important role of His homeostasis in plant development.

Genetic Dissection of Histidine Biosynthesis in Arabidopsis

“…The loss of HISN1A function in homozygotes therefore first becomes critical during root development. Mo et al (2006) observed a similar phenotype in a weak allele (hpa1) of HISN6A and concluded that His performs an important role in root meristem maintenance. An alternative explanation is that HISN6B expression is unable to meet cellular needs for His biosynthesis in root development but can compensate more fully for a loss of HISN6A function elsewhere.…”

“…Disruption of another gene (AGD2) encoding a novel aminotransferase required for Lys biosynthesis (Hudson et al, 2006) also results in embryo lethality (Song et al, 2004). In contrast, weak alleles of HISN3 and HISN6A have a seedling phenotype Mo et al, 2006). Collections of Arabidopsis auxotrophs are not sufficiently robust at present to enable a definitive comparison of knockout phenotypes for each pathway.…”

“…This mutant is altered in the same step of the pathway as the Nicotiana auxotroph. A weak mutant allele of this locus (hpa1) exhibits a short-root phenotype in Arabidopsis that can be rescued by supplemental His (Mo et al, 2006). A mutant disrupted in one of the duplicated HISN1 genes responsible for the first step in the pathway also exhibits a root phenotype (Wang et al, 2005).…”

The ArabidopsisTUMOR PRONE5Gene Encodes an Acetylornithine Aminotransferase Required for Arginine Biosynthesis and Root Meristem Maintenance in Blue Light

“…This phenotype also distinguishes tup5-1 from other Arabidopsis mutants impaired in amino acid biosynthesis or metabolism showing defects in root growth, such as the hpa1 His biosynthesis mutant (Mo et al, 2006), the mutant Rm 57 disturbed in the Lys biosynthetic pathway (Sarrobert et al, 2000), and two mutants of the genes encoding Asp aminotransferase AspAT2, aat2-2 and aat2-T (Schultz et al, 1998;Miesak and Coruzzi, 2002). The His biosynthesis mutant hpa1 resembles tup5-1 insofar as it has a short root when grown in vitro, but there is no obvious phenotype in the aerial part and hpa1 mutants are fully fertile plants (Mo et al, 2006). Mutants for several Trp biosynthetic pathway genes are generally impaired in development under high-light but not under low-light conditions (Last et al, 1991;Radwanski et al, 1996).…”

“…One such example is the characterization of a Trp biosynthesis mutant displaying a severe growth defect under high light by Last et al (1991); another one is the description of a Lys biosynthesis mutant showing altered leaf morphology and mild dwarfism by Song et al (2004). Amino acid metabolism might also influence root meristem maintenance, as well as root growth and development, as was indicated by mutants of Asp and His biosynthesis (Miesak and Coruzzi, 2002;Mo et al, 2006). It is well documented that endogenous factors controlling root growth, such as phytohormones, are often regulated by exogenous signals, for example, by water and nutrient conditions (López-Bucio et al, 2003;Monshausen and Gilroy, 2009), as well as light (Canamero et al, 2006;Tong et al, 2008).…”