Plastome evolution in Santalales involves relaxed selection prior to loss of ndh genes and major boundary shifts of the inverted repeat

Maja Edlund; Benjamin M Anderson; Huei-Jiun Su; Tanner Robison; Marcos A Caraballo-Ortiz; Joshua P Der; Daniel L Nickrent; Gitte Petersen

doi:10.1093/aob/mcae145

Plastome evolution in Santalales involves relaxed selection prior to loss of ndh genes and major boundary shifts of the inverted repeat

Ann Bot. 2024 Aug 30:mcae145. doi: 10.1093/aob/mcae145. Online ahead of print.

Authors

Maja Edlund¹, Benjamin M Anderson², Huei-Jiun Su³, Tanner Robison^{4

5}, Marcos A Caraballo-Ortiz⁶, Joshua P Der⁷, Daniel L Nickrent⁵, Gitte Petersen¹

Affiliations

¹ Department of Ecology, Environment and Plant Sciences, Stockholm University, SE-106 91 Stockholm, Sweden.
² Western Australia Herbarium, Department of Biodiversity, Conservation and Attractions, Locked Bag 104, Bentley Delivery Centre, 6983 Australia.
³ Department of Earth and Life Sciences, University of Taipei, Taipei 100234, Taiwan.
⁴ 121 Boyce Thompson Institute, Ithaca, NY 14853, USA.
⁵ Plant Biology Section, School of Integrative Plant Science, CALS, Cornell University, Ithaca, NY 14853, USA.
⁶ Department of Botany, National Museum of Natural History, Smithsonian Institution, MRC-166, P.O. Box 37012, Washington, DC 22013-7012, USA.
⁷ Department of Biological Science (MH-282), California State University, Fullerton, P.O. Box 6850, Fullerton, CA 92834-6850, USA.

PMID: 39213003
DOI: 10.1093/aob/mcae145

Abstract

Background and aims: Biological aspects of haustorial parasitism have significant effects on the configuration of the plastid genome. Approximately half the diversity of haustorial parasites belongs to the order Santalales, where a clearer picture of plastome evolution in relation to parasitism is starting to emerge. However, in previous studies of plastome evolution there is still a notable under-representation of members from non-parasitic and deep-branching hemiparasitic lineages, limiting evolutionary inference around the time of transition to a parasitic lifestyle. To expand taxon sampling relevant to this transition we therefore targeted three families of non-parasites (Erythropalaceae, Strombosiaceae, and Coulaceae), two families of root-feeding hemiparasites (Ximeniaceae and Olacaceae), and two families of uncertain parasitic status (Aptandraceae and Octoknemaceae). With data from these lineages we aimed to explore plastome evolution in relation to evolution of parasitism.

Methods: From 29 new samples we sequenced and annotated plastomes and the nuclear ribosomal cistron. We examined phylogenetic patterns, plastome evolution, and patterns of relaxed or intensified selection in plastid genes. Available transcriptome data were analyzed to investigate potential transfer of infA to the nuclear genome.

Results: Phylogenetic relationships indicate a single functional loss of all plastid ndh genes (ndhA-K) in a clade formed by confirmed parasites and Aptandraceae, and the loss coincides with major size and boundary shifts of the inverted repeat (IR) region. Depending on an autotrophic or heterotrophic lifestyle in Aptandraceae, plastome changes are either correlated with or predate evolution of parasitism. Phylogenetic patterns also indicate repeated loss of infA from the plastome, and based on presence of transcribed sequences with presequences corresponding to thylakoid luminal transit peptides, we infer that the genes were transferred to the nuclear genome.

Conclusions: Except for the loss of the ndh complex, relatively few genes have been lost from the plastome in deep-branching root parasites in Santalales. Prior to loss of the ndh genes, they show signs of relaxed selection indicative of their dispensability. To firmly establish a potential correlation between ndh gene loss, plastome instability and evolution of parasitism, it is pertinent to refute or confirm a parasitic lifestyle all Santalales clades.

Keywords: Santalales; gene loss; inverted repeat; parasitism; phylogeny; plastome evolution.