Even before losing their ability to photosynthesize, parasitic plants like Balanophora were reshaping their genomes in dramatic ways.
A deep dive into the DNA of seven species from Taiwan and Japan reveals tiny, streamlined plastid genomes that ditched photosynthesis long ago but hung onto genes for other vital tasks, researchers report November 26 in New Phytologist. The study also uncovers how these root-hugging parasites independently evolved seed production without pollination on islands, offering a window into how plants adapt to a life of total dependence on hosts.
Balanophora plants are oddballs in the plant world: they’re holoparasites, meaning they latch onto the roots of host trees and siphon off all their water, nutrients, and energy, skipping photosynthesis entirely. This lifestyle has led to bizarre fungus-like flowers that poke out of the ground only during blooming season, and it’s triggered massive changes in their genomes, especially the plastid — the organelle that in green plants handles photosynthesis via the chloroplast.
Previous glimpses into Balanophora’s plastids came from just a handful of species, showing shrunken genomes stripped of most typical plant genes. To get a fuller picture, the team collected samples from 12 populations across humid forests in Taiwan and Japan, focusing on seven of the eight known species there. They sequenced and assembled the plants’ plastid genomes and nuclear transcriptomes—the active genes from the cell nucleus.
The plastids turned out to be puny, clocking in at 14 to 16 kilobases — about a tenth the size of a typical plant plastid — and packed tight with an extreme bias toward adenine and thymine bases (87-88 percent). They’re all laid out in the same linear order, with a quirky genetic code where the usual “stop” signal TAG codes for the amino acid tryptophan instead. These genomes hold onto just 11 to 13 ribosomal protein genes, four ribosomal RNAs, and one transfer RNA, plus a few others like accD for fatty acid synthesis and clpP for protein chopping.
Phylogenetic trees built from plastid and nuclear genes painted a clear family portrait, grouping the species into four main clades and confirming close ties between Japanese and Taiwanese populations of the same species. The big reveal: the drastic plastid slim-down happened in a common ancestor before the genus diversified, wiping out photosynthesis genes but sparing those for other jobs.
The analysis also spotlighted a reproductive twist. Most Balanophora species are dioecious, with separate male and female plants that need pollination to reproduce sexually. But on islands, several have ditched males altogether, switching to obligate agamospermy—making seeds asexually without fertilization. The trees suggest this happened independently at least twice: once in the lineage leading to B. nipponica on mainland Japan, and again in B. japonica across Japan and Taiwan. “The capacity for agamospermy in Balanophora species with hermaphroditic flowers likely functioned as a preadaptation for the evolution of obligate agamospermy in some species,” the researchers note.
This asexual shift might follow Baker’s Law, where self-reliant reproduction helps plants colonize remote spots like islands. Taiwan and Japan, with their isolated histories, seem to have favored this strategy, allowing single females to establish populations without mates.
Despite the plastid’s minimalism, it’s far from useless. By predicting where nuclear-encoded proteins end up in the cell, the team found over 700 on average headed to the plastid — suggesting it still churns out amino acids, fatty acids, riboflavin, lipoic acid, heme, and isoprenoids, plus bits of glycolysis and the pentose phosphate pathway. “Similar to other parasites, it primarily erased photosynthesis-related functions without massive elimination of other functions,” the authors write.
These insights position Balanophoraceae as a prime model for tracing how plants evolve after ditching sunlight, with implications for understanding genome streamlining in other parasites. As habitats shift, such studies could highlight how dependent species adapt — or falter — in a changing world.
Citations: Phylogenomics clarifies Balanophora evolution, metabolic retention in reduced plastids, and the origins of obligate agamospermy. DOI: 10.1111/nph.70761
