Nuclear—organelle interactions: the immutans variegation mutant of Arabidopsis is plastid autonomous and impaired in carotenoid biosynthesis

Abstract

SummaryThe immutans (ira) variegation mutant of Arabidopsis thaliana contains green-and white-eactored leaves due to the action of a nuclear recessive gene. The mutation is somatically unstable, and the degree of sectoring is Influenced by light and temperature. Whereas the cells in the green sectors contain normal chloroplasts, the cells in the white sectors are heteroplasUdic and contain non-pigmented plastids that lack organized lamellar structures, as well as small pigmented plastids and/or rare normal chloroplasts. This indicates that the plastids in im white cells are not affected equally by the nuclear mutation and that the expression of irnmutans is 'plastid autonomous'. In contrast to other variegation mutants with heteroplastidic cells, the defect in im is not maternally Inherited. immutans thus represents a novel type of nuclear gene-induced variegation mutant. It has also been found that the white tissues of immutans accumulate phytoene, a non-colored C4o carotenoid intermediate. This suggests that immutans controls, either directly or indirectly, the activity of phytoene desaturaea (PDS), the enzyme that converts phytoene to zeta-carotene in higher plants. However, im is not the structural gene for PDS. A secondary effect of carotenoid deficiency, both in immutans and in wildtype plants treated with a herbicide that blocks carotenoid synthesis, is an increase in acid ribonuclease activity in white tissue. It is concluded that the novel variegation generated by the immutans mutation should offer great insight into the complex circuitry that regulates nuclear--organelle interactions.

The Arabidopsis Spontaneous Cell Death1 gene, encoding a ζ-carotene desaturase essential for carotenoid biosynthesis, is involved in chloroplast development, photoprotection and retrograde signalling

“…Because of the substantial loss of carotenoids, spc1-1 has accumulated a higher level of superoxide, which may, at least in part, contribute to the spontaneous cell death phenotype of the mutant. Similar to other carotenoid-deficient mutants [54], the penetrance of spc1-1 mutant phenotype is light dependent, with a stronger mutant phenotype under the high light condition. This light-dependent phenotype is presumably a consequence of the accumulation of more ROS under high light that cannot be efficiently removed owing to a lower level of carotenoid-type antioxidants.…”

“…Moreover, carotenoid deficiency has been reported to cause sharply reduced levels of chlorophyll [54,55]. We therefore measured the chlorophyll levels in the leaves of WT, spc1-1 and spc1-2 plants.…”

Mutations in the Arabidopsis Gene IMMUTANS Cause a Variegated Phenotype by Inactivating a Chloroplast Terminal Oxidase Associated with Phytoene Desaturation

“…When seeds from green sectors were sown, a variety of variegated plants germinated and developed, suggesting that the green phenotype is not caused by a reversion of the mutation ( Figure 1A). This phenotype is reminiscent of the im -conferred phenotype that was described previously as a chloroplast autonomous mutation (Rédei, 1963;Wetzel et al, 1994).The white tissues of im have been shown to lack functional carotenoid and to accumulate phytoene, which is an intermediate compound of the carotenoid biosynthesis pathway. We analyzed the carotenoid content of the variegated albino and compared it with the wild type ( Figure 1B).…”

“…Most of the mutations leading to the accumulation of early intermediates of the pathway are expected to be lethal due to the lack of protection against photooxidation. However, variegated mutants (green/white) can survive because the green tissue provides enough photosynthesis for plant growth and reproduction, allowing the propagation of homozygous mutant plants and thereby permitting the study of chloroplast-deficient (containing white plastids) living tissues.A striking example of such a variegated phenotype is provided by the immutans ( im ) mutant from Arabidopsis (Wetzel et al, 1994). This mutant shows a light-dependent variegated phenotype.…”

Effects of chloroplast dysfunction in a subpopulation of leaf mesophyll cells on photosynthetic and respiratory activities of a whole leaf: A study using variegated leaves of Hedera helix L.

“…The various causes of this variegation include plastid ribosome deficiency (Han et al 1992, Hess et al 1993, alteration of plastid genome (Stoike and Sears 1998), mitochondrial dysfunction (Martínez-Zapater et al 1992, Sakamoto et al 1996, and deficiencies in carotenoid biosynthesis (Wetzel et al 1994). Variegated plants have played prominent roles in research on genetics (e.g., discovery of non-Mendelian inheritance) and morphology (e.g., analysis of cell lineage in leaf development).…”