Dense infraspecific sampling reveals rapid and independent trajectories of plastome degradation in a heterotrophic orchid complex

Craig F. Barrett; Susann Wicke; Chodon Sass

doi:10.1111/nph.15072

Characterization of the complete plastomes of two flowering epiparasites (Phacellaria glomerata and P. compressa, Santalaceae, Santalales): gene content, organization and plastome degradation

10.21203/rs.2.9317/v1 ◽

2019 ◽

Author(s):

Xiaorong Guo ◽

Changkun Liu ◽

Hengchang Wang ◽

Guangfei Zhang ◽

Hanjing Yan ◽

...

Keyword(s):

Plastid Genome ◽

Growth Form ◽

Size Structure ◽

General Pattern ◽

Gene Content ◽

Evolutionary Pathway ◽

Plant Parasite ◽

Content Organization ◽

Plastome Degradation

Abstract Backgrounds: The transition to a heterotrophic lifestyle triggers reductive evolution of plastid genome (plastome) in both photosynthetic and non–photosynthetic parasites. A plant parasite parasitizing another plant parasite is referred to as epiparasitism, which is extremely rare in angiosperms. In despite of the particularly special lifeform of epiparasitic plants, their plastomes have not been characterized to date. Sequending such plastomes may enable new insights into the evolutionary pathway of plastome degradation associated with parasitism. Results: In this study, we generated complete plastomes of Phacellaria compressa and P. glomerata (Santalaceae, Santalales) through Illumina shotgun sequencing. Plastome assembly and comparison indicated that plastomes of both species exhibit the quadripartite structure typical of angiosperms, and that they possess similar size, structure, gene content, and arrangement of genes to other hemiparasites in Santalales, especially to those hemiparasites in Santalaceae. The plastomes of P. compressa and P. glomerata were characterized by the functional loss of plastid–encoded NAD(P)H–dehydrogenase and infA genes, which strongly coincides with the general pattern of plastome degradation observed in Santalales hemiparasites. Conclusion: Our study demonstrates that the shift to epiparasitism and reduced vegetative bodies in P. compressa and P. glomerata do not appear to cause any unique plastome degradation compared with their closely related hemiparasites. The epiparasitic lifestyle or an endophytic growth form observed in these two epiparasites may have limited impact on the reductive modification of their plastomes.

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Diverse trajectories of plastome degradation in holoparasitic Cistanche and genomic location of the lost plastid genes

Journal of Experimental Botany ◽

10.1093/jxb/erz456 ◽

2019 ◽

Vol 71 (3) ◽

pp. 877-892 ◽

Cited By ~ 1

Author(s):

Xiaoqing Liu ◽

Weirui Fu ◽

Yiwei Tang ◽

Wenju Zhang ◽

Zhiping Song ◽

...

Keyword(s):

Purifying Selection ◽

Single Copy ◽

Functional Genes ◽

Coding Region ◽

Plastid Genomes ◽

Plastome Evolution ◽

Genomic Location ◽

Single Genus ◽

Genomic Locations ◽

Plastome Degradation

Abstract The plastid genomes (plastomes) of non-photosynthetic plants generally undergo gene loss and pseudogenization. Despite massive plastomes reported in different parasitism types of the broomrape family (Orobanchaceae), more plastomes representing different degradation patterns in a single genus are expected to be explored. Here, we sequence and assemble the complete plastomes of three holoparasitic Cistanche species (C. salsa, C. mongolica, and C. sinensis) and compare them with the available plastomes of Orobanchaceae. We identified that the diverse degradation trajectories under purifying selection existed among three Cistanche clades, showing obvious size differences in the entire plastome, long single copy region, and non-coding region, and different patterns of the retention/loss of functional genes. With few exceptions of putatively functional genes, massive plastid fragments, which have been lost and transferred into the mitochondrial or nuclear genomes, are non-functional. In contrast to the equivalents of the Orobanche species, some plastid-derived genes with diverse genomic locations are found in Cistanche. The early and initially diverged clades in different genera such as Cistanche and Aphyllon possess obvious patterns of plastome degradation, suggesting that such key lineages should be considered prior to comparative analysis of plastome evolution, especially in the same genus.

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Plastid Genome Degradation in the Endangered, Mycoheterotrophic, North American Orchid Hexalectris warnockii

Genome Biology and Evolution ◽

10.1093/gbe/evy107 ◽

2018 ◽

Vol 10 (7) ◽

pp. 1657-1662 ◽

Cited By ~ 7

Author(s):

Craig F Barrett ◽

Aaron H Kennedy

Keyword(s):

Plastid Genome ◽

Tandem Repeats ◽

Functional Genes ◽

Evolutionary Models ◽

Natural Experiments ◽

Conservation Genetic ◽

Genes Encoding ◽

Plastid Genome Evolution ◽

Plastome Degradation ◽

Genome Degradation

Abstract Heterotrophic plants provide evolutionarily independent, natural experiments in the genomic consequences of radically altered nutritional regimes. Here, we have sequenced and annotated the plastid genome of the endangered mycoheterotrophic orchid Hexalectris warnockii. This orchid bears a plastid genome that is ∼80% the total length of the leafy, photosynthetic Phalaenopsis, and contains just over half the number of putatively functional genes of the latter. The plastid genome of H. warnockii bears pseudogenes and has experienced losses of genes encoding proteins directly (e.g., psa/psb, rbcL) and indirectly involved in photosynthesis (atp genes), suggesting it has progressed beyond the initial stages of plastome degradation, based on previous models of plastid genome evolution. Several dispersed and tandem repeats were detected, that are potentially useful as conservation genetic markers. In addition, a 29-kb inversion and a significant contraction of the inverted repeat boundaries are observed in this plastome. The Hexalectris warnockii plastid genome adds to a growing body of data useful in refining evolutionary models in parasites, and provides a resource for conservation studies in these endangered orchids.

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