Whole-genome Sequencing Reveals Autooctoploidy in Chinese Sturgeon and Its Evolutionary Trajectories

Abstract

The order Acipenseriformes, which includes sturgeons and paddlefishes, represents “living fossils” with complex genomes that are good models for understanding whole-genome duplication (WGD) and ploidy evolution in fishes. Here, we sequenced and assembled the first high-quality chromosome-level genome for the complex octoploid Acipenser sinensis (Chinese sturgeon), a critically endangered species that also represents a poorly understood ploidy group in Acipenseriformes. Our results show that A. sinensis is a complex autooctoploid species containing four kinds of octovalents (8n), a hexavalent (6n), two tetravalents (4n), and a divalent (2n). An analysis taking into account delayed rediploidization reveals that the octoploid genome composition of Chinese sturgeon results from two rounds of homologous WGDs, and further provides insights into the timing of its ploidy evolution. This study provides the first octoploid genome resource of Acipenseriformes for understanding ploidy compositions and evolutionary trajectories of polyploid fishes.

1. Introduction

The order Acipenseriformes, which includes sturgeons and paddlefishes, is an ancient group of fishes with a wide distribution in the Northern Hemisphere. Many species of Acipenseriformes are threatened or endangered, particularly due to their commercial values for meat and caviar. As “living fossils”, Acipenseriformes species retain primitive characteristics (such as a heterocercal tail and cartilaginous skeleton) and occupy the basal position of Actinopterygii phylogeny [1]. They also exhibit a slow rate of evolution [2], complex genomes (half of their chromosomes are micro-chromosomes), and complex ploidy, with the order divisible into three ploidy classifications: Group A (≈120 chromosomes with nuclear DNA content of 3.2–4.6 pg), Group B (≈240 chromosomes with nuclear DNA content of 6.1–9.6 pg), and Group C (≈360 chromosomes with nuclear DNA content of 13.1–14.2 pg) [3,4]. A better understanding of Acipenseriformes could aid in conservation efforts and provide insights into the understanding of whole-genome duplication (WGD) and ploidy evolution in fishes [5–7].

WGDs are very common in the evolution of fishes [8–10], and subsequent rediploidization further increases the complexity of the genomes. Both Acipenseriformes and teleosts (ray-finned fishes except primitive bichirs, sturgeons, paddlefishes, freshwater garfishes, and bowfins) have undergone at least three rounds of WGDs. The first two rounds include the first-round WGD (1R) that occurred ≈600 million years ago (MYA) and a jawed vertebrate-specific second-round WGD (2R) that occurred after the divergence of lamprey and jawed vertebrates. Teleosts then underwent a teleost-specific third-round WGD (Ts3R) [11–14], whereas Acipenseriformes underwent an independent Acipenseriformes-specific third-round WGD (As3R) [11]. Acipenseriformes species are thought to have undergone a delayed rediploidization, in which a species radiates an extensive time after a WGD event (i.e., a timescale on the order of millions of years) [15], resulting in complex ploidies. However, the ploidy compositions of most Acipenseriformes species have been challenging to clarify. The debates regarding ploidy, for example, whether Groups A and B are diploid and tetraploid [5] or are instead tetraploid [16] and octoploid [17–19], or even are paleotetraploidy versus modern/functional diploidy in the case of Group A [4], have lasted for half a century [20,21]. It has been difficult to end the debate solely by relying on traditional DNA content measurements, cytogenetics, and [continued]