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Abstract The inner-envelope K+ EFFLUX ANTIPORTERS (KEA) 1 and 2 are critical for chloroplast development, ion homeostasis, and photosynthesis. However, the mechanisms by which changes in ion flux across the envelope affect organelle biogenesis remained elusive. Chloroplast development requires intricate coordination between the nuclear genome and the plastome. Many mutants compromised in plastid gene expression (PGE) display a virescent phenotype, that is delayed greening. The phenotypic appearance of Arabidopsis thaliana kea1 kea2 double mutants fulfills this criterion, yet a link to PGE has not been explored. Here, we show that a simultaneous loss of KEA1 and KEA2 results in maturation defects of the plastid ribosomal RNAs. This may be caused by secondary structure changes of rRNA transcripts and concomitant reduced binding of RNA-processing proteins, which we documented in the presence of skewed ion homeostasis in kea1 kea2. Consequently, protein synthesis and steady-state levels of plastome-encoded proteins remain low in mutants. Disturbance in PGE and other signs of plastid malfunction activate GENOMES UNCOUPLED 1-dependent retrograde signaling in kea1 kea2, resulting in a dramatic downregulation of GOLDEN2-LIKE transcription factors to halt expression of photosynthesis-associated nuclear-encoded genes (PhANGs). PhANG suppression delays the development of fully photosynthesizing kea1 kea2 chloroplasts, probably to avoid progressing photo-oxidative damage. Overall, our results reveal that KEA1/KEA2 function impacts plastid development via effects on RNA-metabolism and PGE.
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Delayed leaf greening involves a major shift in the expression of cytosolic and mitochondrial ribosomes to plastid ribosomes in the highly phosphorus-use-efficient Hakea prostrata (Proteaceae)
Abstract Background and aimsHakea prostrata(Proteaceae) is a highly phosphorus-use-efficient plant native to southwest Australia. It maintains a high photosynthetic rate at low leaf phosphorus (P) and exhibits delayed leaf greening, a convergent adaptation that increases nutrient-use efficiency. This study aimed to provide broad physiological and gene expression profiles across leaf development, uncovering pathways leading from young leaves as nutrient sinks to mature leaves as low-nutrient, energy-transducing sources. MethodsTo explore gene expression underlying delayed greening, we analysed a de novo transcriptome forH. prostrataacross five stages of leaf development. Photosynthesis and respiration rates, and foliar pigment, P and nitrogen (N) concentrations were determined, including the division of P into five biochemical fractions. Key resultsTranscripts encoding functions associated with leaf structure generally decreased in abundance across leaf development, concomitant with decreases in foliar concentrations of 85% for anthocyanins, 90% for P and 70% for N. The expression of genes associated with photosynthetic function increased during or after leaf expansion, in parallel with increases in photosynthetic pigments and activity, much later in leaf development than in species that do not have delayed greening. As leaves developed, transcript abundance for cytosolic and mitochondrial ribosomal proteins generally declined, whilst transcripts for chloroplast ribosomal proteins increased. ConclusionsThere was a much longer temporal separation of leaf cell growth from chloroplast development inH. prostratathan is found in species that lack delayed greening. Transcriptome-guided analysis of leaf development inH. prostrataprovided insight into delayed greening as a nutrient-saving strategy in severely phosphorus-impoverished landscapes.
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- Award ID(s):
- 1923589
- PAR ID:
- 10479191
- Publisher / Repository:
- Springer Link
- Date Published:
- Journal Name:
- Plant and Soil
- ISSN:
- 0032-079X
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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- Free Publicly Accessible Full Text
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Accepted Manuscript
- Journal Article:
- https://doi.org/10.1007/s11104-023-06275-1
