Abstract
Plastomes of heterotrophs went through varying degrees of degradation along with the transition from autotrophic to heterotrophic lifestyle. Here, we identified the plastome of mycoheterotrophic species Burmannia itoana and compared it with those of its reported relatives including three autotrophs and one heterotroph (Thismia tentaculata) in Dioscoreales. B. itoana yields a rampantly degraded plastome reduced in size and gene numbers at the advanced stages of degradation. Its length is 44,463 bp with a quadripartite structure. B. itoana plastome contains 33 tentatively functional genes and six tentative pseudogenes, including several unusually retained genes. These unusual retention suggest that the inverted repeats (IRs) regions and possibility of being compensated may prolong retention of genes in plastome at the advanced stage of degradation. Otherwise, six rearrangements including four inversions (Inv1/Inv2/Inv3/Inv4) and two translocations (Trans1/Trans2) were detected in B. itoana plastome vs. its autotrophic relative B. disticha. We speculate that Inv1 may be mediated by recombination of distinct tRNA genes, while Inv2 is likely consequence of extreme gene losses due to the shift to heterotrophic lifestyle. The other four rearrangements involved in IRs and small single copy region may attribute to multiple waves of IRs and overlapping inversions. Our study fills the gap of knowledge about plastomes of heterotroph in Burmannia and provides a new evidence for the convergent degradation patterns of plastomes en route to heterotrophic lifestyle.
Highlights
Plastids were derived from a common cyanobacterial ancestor that established a permanent endosymbiotic relationship with mitochondriate ancestor (Gould, Waller & McFadden, 2008; Ku et al, 2015)
The presumably functional genes include four rRNA genes, eight tRNA genes and 21 protein genes, while six genes are identified as putative pseudogenes based on the reasons below: the presence of internal stop codons in petG and rpl36; the anticodon sequences of the trnH_GUG was deleted compared with the typical trnH_GUG; multiple base changes in anticodon and other regions in trnD_GUC compared with the functional trnD_GUC, and no tRNA was predicted by tRNAscan; several indels or substitutes in the trnG_GCC compared with the typical trnG_GCC, and no tRNA was predicted by tRNAscan; several indels or substitutes in the anticodon and other regions of the trmS_UGA compared with the typical trmS_UGA, and no tRNA was predicted by tRNAscan
Based on models of plastome evolution, B. itoana plastome is at the advanced stages of degradation, and occurrence of six putative pseudogenes suggests that it could undergo further degradation
Summary
Plastids were derived from a common cyanobacterial ancestor that established a permanent endosymbiotic relationship with mitochondriate ancestor (Gould, Waller & McFadden, 2008; Ku et al, 2015). Most typical plastomes are variable in size ranging from approximate 120 to 170 kbp with about 113 unique genes including about 79 protein-coding genes, four rRNA genes, and 30 tRNA genes (Wicke et al, 2011). These genes are classified into three main classes depending on functions: (1) photosynthesis related genes (ndh/atp/psa/psb/pet/ycf3/ycf4/rbcL); (2) transcription, transcript maturation, and translation related genes (rpo/infA, matK, and tRNAs/rRNAs/rps/rpl), (3) other non-bioenergetic function genes (accD/clpP/ycf1/ycf2/ccsA/cemA) (Bock, 2007; Wicke et al, 2011)
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