Next‐generation sequencing data suggest that certain nonphotosynthetic green plants have lost their plastid genomes

Smith, David Roy; Asmail, Sara Raad

doi:10.1111/nph.12919

Cited by 15 publications

(10 citation statements)

References 44 publications

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“…Of these, acc D and trn E typically appear to be retained the longest. Plastome‐less mycoheterotrophs may also exist, parallel to reported losses in Polytomella (a heterotrophic alga) and Rafflesia (a holoparasitic angiosperm); see Smith & Asmail (). This prediction is amenable to study by looking for absence of plastid‐targeted nuclear‐encoded genes in genomic data from these organisms.…”

Section: Conclusion: a Modified Model For Plastome Degradation And mentioning

confidence: 97%

Plastomes on the edge: the evolutionary breakdown of mycoheterotroph plastid genomes

2017

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Contents 48I.48II.50III.5354References54 Summary We examine recent evidence for ratchet‐like genome degradation in mycoheterotrophs, plants that obtain nutrition from fungi. Initial loss of the NADH dehydrogenase‐like (NDH) complex may often set off an irreversible evolutionary cascade of photosynthetic gene losses. Genes for plastid‐encoded subunits of RNA polymerase and photosynthetic enzymes with secondary functions (Rubisco and ATP synthase) can persist initially, with nonsynchronous and quite broad windows in the relative timing of their loss. Delayed losses of five core nonbioenergetic genes (especially trnE and accD, which respectively code for glutamyl tRNA and a subunit of acetyl‐CoA carboxylase) probably explain long‐term persistence of heterotrophic plastomes. The observed range of changes of mycoheterotroph plastomes is similar to that of holoparasites, although greater diversity of both probably remains to be discovered. These patterns of gene loss/retention can inform research programs on plastome function.

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Section: Conclusion: a Modified Model For Plastome Degradation And mentioning

confidence: 97%

Plastomes on the edge: the evolutionary breakdown of mycoheterotroph plastid genomes

2017

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“…Several of these colourless algae evolved into parasites, such as the Apicomplexa lineage. Polytomella is a genus of colourless, free‐living unicellular nonphotosynthetic green algae, closely related to the photosynthetic green alga Chlamydomonas reinhardtii . Recently, the plastids of Polytomella spp.…”

Section: Introductionmentioning

confidence: 99%

“…RNA‐seq analysis of Polytomella parva uncovered transcripts for a large set of nuclear encoded, plastid‐targeted enzymes mainly involved in carbohydrate and starch metabolism as well as amino acid and fatty acid biosynthesis . This implies that P. parva has maintained a nonphotosynthetic plastid for metabolic purposes as a specialized anabolic organelle . Therefore, P. parva is an attractive model system for exploring the evolutionary pressure to maintain plastids in the absence photosynthesis.…”

Section: Introductionmentioning

confidence: 99%

Interaction of N‐acetyl‐l‐glutamate kinase with the PII signal transducer in the non‐photosynthetic alga Polytomella parva: Co‐evolution towards a hetero‐oligomeric enzyme

et al. 2019

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During evolution, several algae and plants became heterotrophic and lost photosynthesis; however, in most cases, a nonphotosynthetic plastid was maintained. Among these organisms, the colourless alga Polytomella parva is a special case, as its plastid is devoid of any DNA, but is maintained for specific metabolic tasks carried out by nuclear encoded enzymes. This makes P. parva attractive to study molecular events underlying the transition from autotrophic to heterotrophic lifestyle. Here we characterize metabolic adaptation strategies of P. parva in comparison to the closely related photosynthetic alga Chlamydomonas reinhardtii with a focus on the role of plastid‐localized PII signalling protein. Polytomella parva accumulates significantly higher amounts of most TCA cycle intermediates as well as glutamate, aspartate and arginine, the latter being specific for the colourless plastid. Correlating with the altered metabolite status, the carbon/nitrogen sensory PII signalling protein and its regulatory target N‐acetyl‐l‐glutamate‐kinase (NAGK; the controlling enzyme of arginine biosynthesis) show unique features: They have co‐evolved into a stable hetero‐oligomeric complex, irrespective of effector molecules. The PII signalling protein, so far known as a transiently interacting signalling protein, appears as a permanent subunit of the enzyme NAGK. NAGK requires PII to properly sense the feedback inhibitor arginine, and moreover, PII tunes arginine‐inhibition in response to glutamine. No other PII effector molecules interfere, indicating that the PII‐NAGK system in P. parva has lost the ability to estimate the cellular energy and carbon status but has specialized to provide an entirely glutamine‐dependent arginine feedback control, highlighting the evolutionary plasticity of PII signalling system.

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“…Even more impressive is the mtDNA of the shrub Amborella trichopoda, which harbors the equivalent of six horizontally acquired mitochondrial genomes (84). Until recently, it was thought that plastids were impenetrable to foreign DNA (85,86). However, new data from various angiosperms uncovered mitochondrion-to-plastid (87,88) and nucleusto-plastid DNA migration events (89), and there are also examples of plastids, including those of some diatoms and the red alga Gracilaria tenuistipitata, acquiring genes from plasmid or bacterial genomes (69,90).…”

Section: A Multiplicity Of Mitochondrial and Plastid Genome Architectmentioning

confidence: 99%

Mitochondrial and plastid genome architecture: Reoccurring themes, but significant differences at the extremes

Smith

Keeling

2015

Proc. Natl. Acad. Sci. U.S.A.

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356

344

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Mitochondrial and plastid genomes show a wide array of architectures, varying immensely in size, structure, and content. Some organelle DNAs have even developed elaborate eccentricities, such as scrambled coding regions, nonstandard genetic codes, and convoluted modes of posttranscriptional modification and editing. Here, we compare and contrast the breadth of genomic complexity between mitochondrial and plastid chromosomes. Both organelle genomes have independently evolved many of the same features and taken on similar genomic embellishments, often within the same species or lineage. This trend is most likely because the nuclear-encoded proteins mediating these processes eventually leak from one organelle into the other, leading to a high likelihood of processes appearing in both compartments in parallel. However, the complexity and intensity of genomic embellishments are consistently more pronounced for mitochondria than for plastids, even when they are found in both compartments. We explore the evolutionary forces responsible for these patterns and argue that organelle DNA repair processes, mutation rates, and population genetic landscapes are all important factors leading to the observed convergence and divergence in organelle genome architecture.E ndosymbiosis can dramatically impact cellular and genomic architectures. Mitochondria and plastids exemplify this point. Each of these two types of energy-producing eukaryotic organelle independently arose from the endosymbiosis, retention, and integration of a free-living bacterium into a host cell more than 1.4 billion years ago. Mitochondria came first, evolving from an alphaproteobacterial endosymbiont in an ancestor of all known living eukaryotes, and still exist, in one form or another (1), in all its descendants (2). Plastids came later, via the "primary" endosymbiosis of a cyanobacterium by the eukaryotic ancestor of the Archaeplastida, and then spread laterally to disparate groups through eukaryote-eukaryote endosymbioses (3). Consequently, a significant proportion of the identified eukaryotic diversity has a plastid.With few exceptions (1, 4), mitochondria and plastids contain genomes-chromosomal relics of the bacterial endosymbionts from which they evolved (2, 5). Mitochondrial and plastid DNAs (mtDNAs and ptDNAs) have many traits in common, which is not surprising given their similar evolutionary histories. Both are highly reduced relative to the genomes of extant, free-living alphaproteobacteria and cyanobacteria (2, 5), and both have transferred most of their genes to the host nuclear genome and are therefore reliant on nuclear-encoded, organelle-targeted proteins for the preservation of crucial biochemical pathways and many repair-, replication-, and expression-related functions (6). Both also show a wide and perplexing assortment of genomic architectures (7,8), which has spurred various evolutionary explanations, ranging from ancient inheritance from the RNA world to selection for greater "evolvability" (9, 10).At first glance, genomic complexity w...

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Next‐generation sequencing data suggest that certain nonphotosynthetic green plants have lost their plastid genomes

Cited by 15 publications

References 44 publications

Plastomes on the edge: the evolutionary breakdown of mycoheterotroph plastid genomes

Plastomes on the edge: the evolutionary breakdown of mycoheterotroph plastid genomes

Interaction of N‐acetyl‐l‐glutamate kinase with the PII signal transducer in the non‐photosynthetic alga Polytomella parva: Co‐evolution towards a hetero‐oligomeric enzyme

Mitochondrial and plastid genome architecture: Reoccurring themes, but significant differences at the extremes

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