Plastid-nucleus retrograde signaling (PNRS) play essential roles in regulating nuclear gene expression during plant growth and development. Excessive reactive oxygen species can trigger PNRS. We previously reported that in apple (Malus domestica Borkh.) seedlings, the expression of microRNA156 (miR156) was significantly low in the adult phase, which was accompanied by high levels of hydrogen peroxide (H₂O₂) accumulation in chloroplasts. However, it was unclear whether adult-phase-specific chloroplast H₂O₂ may induce PNRS and affect miR156 expression, or miR156 triggers adult phase PNRS during the ontogenesis. In this paper, we examined the relationship between miR156 levels and six PNRS components in juvenile and adult phase leaves from ‘Zisai Pearl’בRed Fuji’ hybrids. We found that PNRS generated by singlet oxygen (¹O₂), the photosynthetic redox state, methylerythritol cyclodiphosphate (MEcPP), SAL1-3-phosphoadenosine 5-phosphate (PAP) and WHIRLY1 were not involved. The accumulation of Mg-protoporphyrin IX (Mg-Proto IX), the expression of the synthetic genes MdGUN5 and MdGUN6, and Mg-Proto IX PNRS related nuclear genes increased with ontogenesis. These changes were negatively correlated with miR156 expression. Manipulating Mg-Proto IX synthesis with 5-aminolevulinic acid (ALA) or gabaculine did not affect miR156 expression in vitro shoots. In contrast, modulating miR156 expression via MdGGT1 or MdMIR156a6 transgenesis led to changes in Mg-Proto IX contents and the corresponding gene expressions. It was concluded that the Mg-Proto IX PNRS was regulated downstream of miR156 regardless of adult-phase-specific plastid H₂O₂ accumulation. The findings may facilitate the understanding of the mechanism of ontogenesis in higher plants.

中文翻译：

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MicroRNA156（miR156）对Mg-原卟啉IX（Mg-原IX）的生物合成及其质体-核逆行信号产生负面影响。

质体核逆行信号（PNRS）在植物生长发育过程中调节核基因表达中起着重要作用。活性氧过多会触发PNRS。我们以前曾报道苹果（Malus domestica Borkh。）幼苗中，成年期microRNA156（miR156）的表达明显较低，这伴随着叶绿体中高水平的过氧化氢（H ₂ O ₂）积累。但是，尚不清楚是否有成年期特定的叶绿体H ₂ O ₂可能会诱导PNRS并影响miR156的表达，或者miR156在本体形成过程中触发成年期PNRS。在本文中，我们研究了“自斋珍珠”ד红富士”杂种的幼年和成年期叶片中miR156水平与六个PNRS成分之间的关​​系。我们发现由单线态氧（¹ O ₂），光合作用的氧化还原态，甲基赤藓糖醇环二磷酸（MEcPP），SAL1-3-磷酸腺苷5-磷酸（PAP）和WHIRLY1生成的PNRS不参与其中。Mg-原卟啉IX（Mg-Proto IX）的积累，合成基因MdGUN5和MdGUN6的表达，和Mg-Proto IX PNRS相关的核基因随着个体发生而增加。这些变化与miR156表达负相关。用5-氨基乙酰丙酸（ALA）或加巴卡环处理Mg-Proto IX合成不会影响miR156体外芽的表达。相反，通过MdGGT1或MdMIR156a6转基因调节miR156表达导致Mg-Proto IX含量和相应基因表达的变化。结论是，无论成年期特异性质体H ₂ O _2的积累如何，Mg-Proto IX PNRS都在miR156下游受到调控。这些发现可能有助于理解高等植物的本体发生机理。