Exceptional reduction of the plastid genome of saguaro cactus (Carnegiea gigantea): Loss of the ndh gene suite and inverted repeat 1

Michael J. Sanderson, Dario Copetti, Alberto Búrquez, Enriquena Bustamante, Joseph L M Charboneau, Luis E. Eguiarte, Sudhir Kumar, Hyun Oh Lee, Junki Lee, Michelle McMahon, Kelly Steele, Rod Wing, Tae Jin Yang, Derrick Zwickl, Martin Wojciechowski

Research output: Contribution to journalArticle

42 Citations (Scopus)

Abstract

PREMISE OF THE STUDY: Land-plant plastid genomes have only rarely undergone signifi cant changes in gene content and order. Thus, discovery of additional examples adds power to tests for causes of such genome-scale structural changes. METHODS: Using next-generation sequence data, we assembled the plastid genome of saguaro cactus and probed the nuclear genome for transferred plastid genes and functionally related nuclear genes. We combined these results with available data across Cactaceae and seed plants more broadly to infer the history of gene loss and to assess the strength of phylogenetic association between gene loss and loss of the inverted repeat (IR). KEY RESULTS: The saguaro plastid genome is the smallest known for an obligately photosynthetic angiosperm (~113 kb), having lost the IR and plastid ndh genes. This loss supports a statistically strong association across seed plants between the loss of ndh genes and the loss of the IR. Many nonplastid copies of plastid ndh genes were found in the nuclear genome, but none had intact reading frames; nor did three related nuclear-encoded subunits. However, nuclear pgr5, which functions in a partially redundant pathway, was intact. CONCLUSIONS: The existence of an alternative pathway redundant with the function of the plastid NADH dehydrogenase-like complex (NDH) complex may permit loss of the plastid ndh gene suite in photoautotrophs like saguaro. Loss of these genes may be a recurring mechanism for overall plastid genome size reduction, especially in combination with loss of the IR.

Original languageEnglish (US)
Pages (from-to)1115-1127
Number of pages13
JournalAmerican Journal of Botany
Volume102
Issue number7
DOIs
StatePublished - Jul 1 2015

Fingerprint

Carnegiea gigantea
Plastid Genomes
Cactaceae
cactus
plastid
genome
gene
Plastids
Genes
plastids
genes
Spermatophytina
nuclear genome
Seeds
Genome
Embryophyta
Plant Genome
loss
plastid genome
NADH Dehydrogenase

Keywords

  • Cactaceae
  • Cacti
  • Carnegiea gigantea
  • Inverted repeat
  • Ndh genes
  • Phylogenomics
  • Saguaro

ASJC Scopus subject areas

  • Plant Science
  • Ecology, Evolution, Behavior and Systematics
  • Genetics

Cite this

Exceptional reduction of the plastid genome of saguaro cactus (Carnegiea gigantea) : Loss of the ndh gene suite and inverted repeat 1. / Sanderson, Michael J.; Copetti, Dario; Búrquez, Alberto; Bustamante, Enriquena; Charboneau, Joseph L M; Eguiarte, Luis E.; Kumar, Sudhir; Lee, Hyun Oh; Lee, Junki; McMahon, Michelle; Steele, Kelly; Wing, Rod; Yang, Tae Jin; Zwickl, Derrick; Wojciechowski, Martin.

In: American Journal of Botany, Vol. 102, No. 7, 01.07.2015, p. 1115-1127.

Research output: Contribution to journalArticle

Sanderson, MJ, Copetti, D, Búrquez, A, Bustamante, E, Charboneau, JLM, Eguiarte, LE, Kumar, S, Lee, HO, Lee, J, McMahon, M, Steele, K, Wing, R, Yang, TJ, Zwickl, D & Wojciechowski, M 2015, 'Exceptional reduction of the plastid genome of saguaro cactus (Carnegiea gigantea): Loss of the ndh gene suite and inverted repeat 1', American Journal of Botany, vol. 102, no. 7, pp. 1115-1127. https://doi.org/10.3732/ajb.1500184
Sanderson, Michael J. ; Copetti, Dario ; Búrquez, Alberto ; Bustamante, Enriquena ; Charboneau, Joseph L M ; Eguiarte, Luis E. ; Kumar, Sudhir ; Lee, Hyun Oh ; Lee, Junki ; McMahon, Michelle ; Steele, Kelly ; Wing, Rod ; Yang, Tae Jin ; Zwickl, Derrick ; Wojciechowski, Martin. / Exceptional reduction of the plastid genome of saguaro cactus (Carnegiea gigantea) : Loss of the ndh gene suite and inverted repeat 1. In: American Journal of Botany. 2015 ; Vol. 102, No. 7. pp. 1115-1127.
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abstract = "PREMISE OF THE STUDY: Land-plant plastid genomes have only rarely undergone signifi cant changes in gene content and order. Thus, discovery of additional examples adds power to tests for causes of such genome-scale structural changes. METHODS: Using next-generation sequence data, we assembled the plastid genome of saguaro cactus and probed the nuclear genome for transferred plastid genes and functionally related nuclear genes. We combined these results with available data across Cactaceae and seed plants more broadly to infer the history of gene loss and to assess the strength of phylogenetic association between gene loss and loss of the inverted repeat (IR). KEY RESULTS: The saguaro plastid genome is the smallest known for an obligately photosynthetic angiosperm (~113 kb), having lost the IR and plastid ndh genes. This loss supports a statistically strong association across seed plants between the loss of ndh genes and the loss of the IR. Many nonplastid copies of plastid ndh genes were found in the nuclear genome, but none had intact reading frames; nor did three related nuclear-encoded subunits. However, nuclear pgr5, which functions in a partially redundant pathway, was intact. CONCLUSIONS: The existence of an alternative pathway redundant with the function of the plastid NADH dehydrogenase-like complex (NDH) complex may permit loss of the plastid ndh gene suite in photoautotrophs like saguaro. Loss of these genes may be a recurring mechanism for overall plastid genome size reduction, especially in combination with loss of the IR.",
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AU - Copetti, Dario

AU - Búrquez, Alberto

AU - Bustamante, Enriquena

AU - Charboneau, Joseph L M

AU - Eguiarte, Luis E.

AU - Kumar, Sudhir

AU - Lee, Hyun Oh

AU - Lee, Junki

AU - McMahon, Michelle

AU - Steele, Kelly

AU - Wing, Rod

AU - Yang, Tae Jin

AU - Zwickl, Derrick

AU - Wojciechowski, Martin

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N2 - PREMISE OF THE STUDY: Land-plant plastid genomes have only rarely undergone signifi cant changes in gene content and order. Thus, discovery of additional examples adds power to tests for causes of such genome-scale structural changes. METHODS: Using next-generation sequence data, we assembled the plastid genome of saguaro cactus and probed the nuclear genome for transferred plastid genes and functionally related nuclear genes. We combined these results with available data across Cactaceae and seed plants more broadly to infer the history of gene loss and to assess the strength of phylogenetic association between gene loss and loss of the inverted repeat (IR). KEY RESULTS: The saguaro plastid genome is the smallest known for an obligately photosynthetic angiosperm (~113 kb), having lost the IR and plastid ndh genes. This loss supports a statistically strong association across seed plants between the loss of ndh genes and the loss of the IR. Many nonplastid copies of plastid ndh genes were found in the nuclear genome, but none had intact reading frames; nor did three related nuclear-encoded subunits. However, nuclear pgr5, which functions in a partially redundant pathway, was intact. CONCLUSIONS: The existence of an alternative pathway redundant with the function of the plastid NADH dehydrogenase-like complex (NDH) complex may permit loss of the plastid ndh gene suite in photoautotrophs like saguaro. Loss of these genes may be a recurring mechanism for overall plastid genome size reduction, especially in combination with loss of the IR.

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KW - Cacti

KW - Carnegiea gigantea

KW - Inverted repeat

KW - Ndh genes

KW - Phylogenomics

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