Paper · 2022 · PLANT PHYSIOLOGY

Gene co-expression reveals the modularity and integration of C4 and CAM in Portulaca

Ian S Gilman; Jose J Moreno-Villena; Zachary R Lewis; et al.

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claims
5
verbatim quotes
43
citations
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research areas
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Open access

Abstract

C4 photosynthesis and Crassulacean acid metabolism (CAM) have been considered as largely independent adaptations despite sharing key biochemical modules. Portulaca is a geographically widespread clade of over 100 annual and perennial angiosperm species that primarily use C4 but facultatively exhibit CAM when drought stressed, a photosynthetic system known as C4 + CAM. It has been hypothesized that C4 + CAM is rare because of pleiotropic constraints, but these have not been deeply explored. We generated a chromosome-level genome assembly of Portulaca amilis and sampled mRNA from P. amilis and Portulaca oleracea during CAM induction. Gene co-expression network analyses identified C4 and CAM gene modules shared and unique to both Portulaca species. A conserved CAM module linked phosphoenolpyruvate carboxylase to starch turnover during the day-night transition and was enriched in circadian clock regulatory motifs in the P. amilis genome. Preservation of this co-expression module regardless of water status suggests that Portulaca constitutively operate a weak CAM cycle that is transcriptionally and posttranscriptionally upregulated during drought. C4 and CAM mostly used mutually exclusive genes for primary carbon fixation, and it is likely that nocturnal CAM malate stores are shuttled into diurnal C4 decarboxylation pathways, but we found evidence that metabolite cycling may occur at low levels. C4 likely evolved in Portulaca through co-option of redundant genes and integration of the diurnal portion of CAM. Thus, the ancestral CAM system did not strongly constrain C4 evolution because photosynthetic gene networks are not co-regulated for both daytime and nighttime functions.

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Claims 5

Method / resourceobservedoriginal resultpositivemeasured

Claim · model-written summary

A chromosome-level genome assembly of Portulaca amilis was generated.

Taxon
Portulaca amilisPortulaca amilise0
Outcome
chromosome-level genome assemblye0
Value
chromosome-levele0

Organisms pictured · Representative pictures of the matched species, not figures from the paper.

Portulaca amilis
Portulaca amilis · TaxonHans Hillewaert · CC BY-SA 3.0 · Wikimedia Commons ↗

Verbatim

e0

“We generated a chromosome-level genome assembly of Portulaca amilis”

✓ located verbatim in the source · abstract, characters 495–562 · show in text ↑
Observationobservedoriginal resultmeasured

Claim · model-written summary

Co-expression analysis identified shared and unique C4 and CAM gene modules in two Portulaca species.

Taxon
PortulacaPortulacae0
Outcome
C4 and CAM gene modules shared and uniquee0

Organisms pictured · Representative pictures of the matched species, not figures from the paper.

Portulaca
Portulaca · Taxon · picture of the genus (one of its species)Eric Guinther / Marshman at en.wikipedia · CC BY-SA 3.0 · Wikimedia Commons ↗

Verbatim

e0

“Gene co-expression network analyses identified C4 and CAM gene modules shared and unique to both Portulaca species.”

✓ located verbatim in the source · abstract, characters 640–755 · show in text ↑
Observationobservedoriginal resultmeasured

Claim · model-written summary

The conserved CAM module was enriched in circadian clock regulatory motifs.

Taxon
P. amilisPortulaca amilise0
Outcome
circadian clock regulatory motifse0

Organisms pictured · Representative pictures of the matched species, not figures from the paper.

Portulaca amilis
Portulaca amilis · TaxonHans Hillewaert · CC BY-SA 3.0 · Wikimedia Commons ↗

Verbatim

e0

“was enriched in circadian clock regulatory motifs in the P. amilis genome”

✓ located verbatim in the source · abstract, characters 873–946 · show in text ↑
Mechanismauthor interpretationoriginal resultmeasured

Claim · model-written summary

Module preservation across water states suggested constitutive weak CAM activity with drought upregulation.

Taxon
PortulacaPortulacae0
Treatment
droughte0
Outcome
weak CAM cyclee0
Qualifier
regardless of water statuse0

Organisms pictured · Representative pictures of the matched species, not figures from the paper.

Portulaca
Portulaca · Taxon · picture of the genus (one of its species)Eric Guinther / Marshman at en.wikipedia · CC BY-SA 3.0 · Wikimedia Commons ↗

Verbatim

e0

“Preservation of this co-expression module regardless of water status suggests that Portulaca constitutively operate a weak CAM cycle that is transcriptionally and posttranscriptionally upregulated during drought.”

✓ located verbatim in the source · abstract, characters 948–1160 · show in text ↑
Mechanismauthor interpretationoriginal resultmeasured

Claim · model-written summary

The authors inferred C4 evolution by redundant gene co-option and integration of diurnal CAM.

Taxon
PortulacaPortulacae0
Outcome
C4 likely evolvede0
Qualifier
co-option of redundant genes and integration of the diurnal portion of CAMe0

Organisms pictured · Representative pictures of the matched species, not figures from the paper.

Portulaca
Portulaca · Taxon · picture of the genus (one of its species)Eric Guinther / Marshman at en.wikipedia · CC BY-SA 3.0 · Wikimedia Commons ↗

Verbatim

e0

“C4 likely evolved in Portulaca through co-option of redundant genes and integration of the diurnal portion of CAM”

✓ located verbatim in the source · abstract, characters 1414–1527 · show in text ↑