Regulatory Shifts in Plastid Transcription Play a Key Role in Morphological Conversions of Plastids during Plant Development

Abstract

Plastids display a high morphological and functional diversity. Starting from an undifferentiated small proplastid, these plant cell organelles can develop into four major forms: etioplasts in the dark, chloroplasts in green tissues, chromoplasts in colored flowers and fruits and amyloplasts in roots. The various forms are interconvertible into each other depending on tissue context and respective environmental condition. Research of the last two decades uncovered that each plastid type contains its own specific proteome that can be highly different from that of the other types. Composition of these proteomes largely defines the enzymatic functionality of the respective plastid. The vast majority of plastid proteins is encoded in the nucleus and must be imported from the cytosol. However, a subset of proteins of the photosynthetic and gene expression machineries are encoded on the plastid genome and are transcribed by a complex transcriptional apparatus consisting of phage-type nuclear-encoded RNA polymerases and a bacterial-type plastid-encoded RNA polymerase. Both types recognize specific sets of promoters and transcribe partly over-lapping as well as specific sets of genes. Here we summarize the current knowledge about the sequential activity of these plastid RNA polymerases and their relative activities in different types of plastids. Based on published plastid gene expression profiles we hypothesize that each conversion from one plastid type into another is either accompanied or even preceded by significant changes in plastid transcription suggesting that these changes represent important determinants of plastid morphology and protein composition and, hence, the plastid type.

A chloroplast retrograde signal, 3’-phosphoadenosine 5’-phosphate, acts as a secondary messenger in abscisic acid signaling in stomatal closure and germination

“…This raises an open question as to whether combinatorial chloroplastic oxidative stresses, such as drought and high light, might lead to more rapid or enhanced PAP signaling to regulate stomata in conjunction with ABA. Interestingly, the role of PAP in ABA signaling in mature seeds suggests that PAP could also be a signal from small, non-photosynthetic immature plastids which de-differentiated from chloroplasts during seed desiccation (Mansfield et al, 1991; Mansfield and Briarty, 1992; Liebers et al, 2017). The regulation of PAP-ABA interaction might occur differently in seeds compared to guard cells, since PAP accumulation appears to be regulated more by SAL1 abundance than chloroplast redox in seeds.

10.7554/eLife.23361.018Figure 9.Model for fine-tuning of stomatal closure by PAP retrograde signaling.Proposed intersection between PAP and ABA signaling during drought stress, or in ost1 -2 sal1 -8 / abi1 -1 sal1 -8 treated with ABA.

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Extrachloroplastic PP7L Functions in Chloroplast Development and Abiotic Stress Tolerance

“…The SCO class appears not to have a common specific function that causes the cotyledon-specific mutant phenotypes, because its members include proteins involved in different processes, such as plastid protein translation (SCO1; Albrecht et al, 2006), folding of Cys-rich thylakoid proteins (SCO2/CYO1; Shimada et al, 2007), or association with microtubules and the peroxisome (SCO3; Albrecht et al, 2010). Seeds of many oilseed plants like Arabidopsis are green due to the presence of photosynthetically active chloroplasts during embryogenesis, which dedifferentiate into nonphotosynthetic eoplasts during the desiccation phase (Liebers et al, 2017). Immature green sco embryos dissected from siliques are green (Ruppel and Hangarter, 2007;Albrecht et al, 2008Albrecht et al, , 2010, and precocious germination of sco2 and sco3 mutants rescues their sco cotyledon phenotype (Albrecht et al, 2008(Albrecht et al, , 2010.…”

“…In true leaves, chloroplasts develop from meristematic proplastids when the leaf primordia emerge; in cotyledons, chloroplasts develop from proplastids/ eoplasts or etioplasts present in mesophyll tissue within the embryo (Waters and Langdale, 2009;Liebers et al, 2017). These precursors are rapidly converted into chloroplasts upon exposure to light.…”

Systematic sequencing of chloroplast transcript termini fromArabidopsis thalianareveals >200 transcription initiation sites and the extensive imprints of RNA-binding proteins and secondary structures

“…These TSS are created by two RNA polymerase types, a bacterial-like, plastid-encoded RNA polymerase (PEP) and two phagelike, nucleus-encoded, RNA polymerases (NEP). NEP and PEP operate simultaneously, however our samples were taken from tissue populated by mature chloroplasts, where PEP activity predominates (85). Since NEP transcription primarily occurs during early differentiation, the TSS we describe likely underestimate the number of promoters utilized over the course of chloroplast differentiation.…”