Chloroplast Photooxidation-Induced Transcriptome Reprogramming in Arabidopsis<i>immutans</i>White Leaf Sectors

Aluru, Maneesha; Żola, Jarosław; Foudree, Andrew; Rodermel, Steven R.

doi:10.1104/pp.109.135780

Cited by 87 publications

(124 citation statements)

References 92 publications

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“…By contrast, the meta-analysis revealed that IM did appear to be strongly regulated by development in Arabidopsis (Rosso et al, 2006). This is consistent with the observations of Aluru et al (2001Aluru et al ( , 2009 who suggested that IM is required to protect against the potential for photooxidation during the development of chloroplasts, amyloplasts, and etioplasts. Wu et al (1999) proposed that the presence of white sectors in im plants occurs because IM plays a critical role in carotenoid biosynthesis due to its ability to oxidize the PQ pool.…”

Section: Introductionsupporting

confidence: 87%

“…If the PQ pool remains reduced due to the lack of IM, carotenoid biosynthesis is blocked at the phytoene desaturase step, phytoene accumulates, and photobleaching results from an increase in chloroplastic ROS (Wetzel et al, 1994;Wu et al, 1999). Consistent with the notion that white sectoring is triggered by photooxidation (Aluru et al, 2009) is the fact that the variegated phenotype can be suppressed in im plants when grown under low-light conditions (Ré dei, 1963;Wetzel et al, 1994;Aluru and Rodermel, 2004;Rosso et al, 2006).…”

Section: Introductionmentioning

confidence: 70%

“…Light initially trapped and transformed through extremely fast, temperature-insensitive photochemistry (in the femtosecond [10 215 s] to nanosecond [10 29 s] time scale) represents the ultimate form of energy used through much slower, temperature-dependent biochemical processes (ms [10 23 s] to s to h time scales) to maintain cellular homeostasis, growth, and development in all photoautotrophs. Thus, imbalances between photochemistry and redox biochemistry result in modulation of the redox state of the PQ pool of PET (Figure 1) as well as the redox state of the ubiquinone pool of mitochondria ( Figure 12B), indicating that information regarding energy imbalance is transferred between chloroplasts and mitochondria (Noctor et al, 2007;Aluru et al, 2009). Furthermore, we conclude that variegation governed by the redox state of the PET chain is not restricted to im, but rather, also appears to govern variegation in spotty, var1, and var2 (Figure 8; see Supplemental Figure 4 online).…”

Section: Discussionmentioning

confidence: 99%

“…Thus, this raises an important developmental question as to how a photoautotroph mitigates the potential damaging effects of photooxidation during the biogenesis and assembly of its photosystems prior to the establishment of a fully functional photosynthetic apparatus. Important photoprotective mechanisms during chloroplast biogenesis include transient stimulation of nonphotochemical dissipation of excess energy through the xanthophyll cycle (Murchie et al, 2009) as shown during early greening in barley (Hordeum vulgare; Krol et al, 1999) as well as the induction of myriad plant oxidative stress genes including AOX (Aluru et al, 2009).…”

Section: Discussionmentioning

confidence: 99%

“…However, we do not wish to imply that photoprotection through IM as a plastoquinol oxidase is the only mechanism induced during normal chloroplast biogenesis in Arabidopsis. The role of IM as a plastoquinol oxidase must be integrated over time with nonphotochemical quenching (Krol et al, 1999;Falkowski and Chen, 2003;Murchie et al, 2009), and the induction of antioxidant stress genes to prevent photooxidation during chloroplast biogenesis (Aluru et al, 2009).…”

Section: Discussionmentioning

confidence: 99%

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Photosynthetic Redox Imbalance Governs Leaf Sectoring in theArabidopsis thalianaVariegation Mutantsimmutans,spotty,var1, andvar2

et al. 2009

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We hypothesized that chloroplast energy imbalance sensed through alterations in the redox state of the photosynthetic electron transport chain, measured as excitation pressure, governs the extent of variegation in the immutans mutant of Arabidopsis thaliana. To test this hypothesis, we developed a nondestructive imaging technique and used it to quantify the extent of variegation in vivo as a function of growth temperature and irradiance. The extent of variegation was positively correlated (R 2 = 0.750) with an increase in excitation pressure irrespective of whether high light, low temperature, or continuous illumination was used to induce increased excitation pressure. Similar trends were observed with the variegated mutants spotty, var1, and var2. Measurements of greening of etiolated wild-type and immutans cotyledons indicated that the absence of IMMUTANS increased excitation pressure twofold during the first 6 to 12 h of greening, which led to impaired biogenesis of thylakoid membranes. In contrast with IMMUTANS, the expression of its mitochondrial analog, AOX1a, was transiently upregulated in the wild type but permanently upregulated in immutans, indicating that the effects of excitation pressure during greening were also detectable in mitochondria. We conclude that mutations involving components of the photosynthetic electron transport chain, such as those present in immutans, spotty, var1, and var2, predispose Arabidopsis chloroplasts to photooxidation under high excitation pressure, resulting in the variegated phenotype.

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