New insights into the regulation of greening and carbon-nitrogen balance by sugar metabolism through a plastidic invertase

Abstract

Since the photosynthetic apparatus of plants contains a massive amount of nitrogen, the regulation of its development by sugar signals is important to the maintenance of the carbon-nitrogen balance. Recently, we isolated a new Arabidopsis mutant, sicy (sugar-inducible cotyledon yellow)-192, whose cotyledons were prevented from greening by treatment with sucrose. On treatment with sucrose, the expression of photosynthesis-and nitrogen assimilation-related genes was respectively weaker and stronger in the mutant seedlings than the wild-type seedlings. In the mutants, the gene encoding plastidic alkaline/neutral (A/N) invertase (INV-E) was point-mutated at codon 294, with Tyr substituted for Cys (C294Y). These findings provide new insights into the regulation of greening and carbon-nitrogen balance by sugar metabolism through INV-E in plastids. In this addendum, we describe the phenotypes of sicy-192 on treatment with sucrose in more detail, and propose a possible relationship among sugar metabolism through INV-E, plastid-tonucleus retrograde signaling, and ethylene, a plant hormone, in the regulation of plant development and metabolism.The photosynthetic apparatus contains a massive amount of nitrogen and so its development closely depends on the distribution of nitrogen in plants. The system for regulating the distribution of nitrogen via sugar signaling appears to be important for the adjustment of primary metabolism to ensure growth, survival and completion of the life cycle in plants. Therefore, the New insights into the regulation of greening and carbon-nitrogen balance by sugar metabolism through a plastidic invertase 1 On treatment with sucrose, the expression of photosynthesis-related genes was weaker in the mutant than wild-type seedlings, while the activity of nitrate reductase was stronger in the mutant. In the sicy-192 plants, the gene encoding plastidic alkaline/neutral (A/N) invertase (INV-E) was point-mutated at codon 294, with Tyr substituted for Cys (C294Y), but a recombinant INV-E:C294Y protein had the same enzymatic activity and substrate specificity as a recombinant is a recessive but gain-of-function mutant and the protein level and activity, but not the transcript level, of INV-E were increased in the mutant, suggesting that the point mutation enhances the stability of INV-E. These findings provide new insights into the regulation of greening and carbonnitrogen balance by sugar metabolism through INV-E in plastids.1 In this addendum, we describe the effects of treatment with sucrose and plant hormones on the greening of sicy-192 mutants in detail, and discuss how INV-E is involved in the regulation of plant development and metabolism.One interesting feature of sicy-192 was that the greening was inhibited only in early seedlings in the Murashige & Skoog (MS) medium with sucrose (Suc + medium). As

A gain‐of‐function mutation of plastidic invertase alters nuclear gene expression with sucrose treatment partially via GENOMES UNCOUPLED1‐mediated signaling

“…a). On the other, the cotyledons of sicy‐192 mutants became yellow with the Suc treatment at the early stage of seedling development, which was consistent with previous reports (Maruta et al ., ; Tamoi et al ., ). Interestingly, the phenotype of the sicy‐192 mutant was markedly enhanced by the gun1‐101 mutation (Fig.…”

“…The sicy‐192 mutant had a yellow leaf phenotype when treated with Suc at early stage of seedling development only (Maruta et al ., ). An Arabidopsis mutant lacking sigma factor 6 (SIG6), which is a major subunit of plastid‐encoded RNA polymerase (PEP) and essential for the transcription of photosynthesis‐related genes encoded by the plastid genome, also exhibited a cotyledon‐specific pale green phenotype (Ishizaki et al ., ).…”

“…SCO1 encodes the plastidic elongation factor G (EF‐G), and is involved in the translation of photosynthesis‐related genes encoded by the plastid genome. Thus, the phenotypes of these PGE mutants are similar to those of the sicy‐192 mutant, except that greening inhibition in the sicy‐192 mutant only occurs when treated with sugars (Maruta et al ., ; Tamoi et al ., ). Furthermore, we previously found that levels of the rbcL protein (the large subunit of ribulose‐1,5‐bisphosphate carboxylase/oxygenase) encoded by the plastid genome as well as enzymes related to photosynthesis encoded by the nuclear genome was suppressed in the sicy‐192 mutant when treated with Suc (Tamoi et al ., ).…”

HbNIN2, a cytosolic alkaline/neutral‐invertase, is responsible for sucrose catabolism in rubber‐producing laticifers of Hevea brasiliensis (para rubber tree)

“…Emerging evidence bears this out. In Arabidopsis, A/N‐Invs have been revealed to have key functions in signaling transductions (Lou et al ., ), root growth (Barratt et al ., ), photosynthetic apparatus development and nitrogen assimilation (Maruta et al ., ; Tamoi et al ., ), and oxidative stress defense (Xiang et al ., ). In rice, an A/N‐Inv (OsCYT‐INV1) is essential for normal seed‐setting and sucrose utilization in the root (Jia et al ., ), while in Lotus japonicus , one A/N‐Inv (LjINV1) is crucial for whole plant development (Welham et al ., ).…”

Systematic Analysis of Alkaline/Neutral Invertase Genes Reveals the Involvement of Smi-miR399 in Regulation of SmNINV3 and SmNINV4 in Salvia miltiorrhiza

“…Double mutation of AT1G35580 and AT4G09510 ( A/N-InvI ) resulted in drastically reduced root growth and abnormal cell enlargement [26]. Point-mutation of AT5G22510 ( A/N-InvE ) inhibited photosynthetic apparatus development and enhanced nitrate assimilation in Arabidopsis seedlings treated with sugar [27,28]. Mutation of AT3G05820 ( A/N-InvH ) caused severe reduction of shoot growth and delay in the first stage of flowering [29].…”