Inferring the Origin of Cultivated Zizania latifolia, an Aquatic Vegetable of a Plant-Fungus Complex in the Yangtze River Basin

Abstract

Crop domestication is one of the essential topics in evolutionary biology. Cultivated Zizania latifolia, domesticated as the special form of a plant-fungus (the host Zizania latifolia and the endophyte Ustilago esculenta) complex, is a popular aquatic vegetable endemic in East Asia. The rapid domestication of cultivated Z. latifolia can be traced in the historical literature but still need more evidence. This study focused on deciphering the genetic relationship between wild and cultivated Z. latifolia, as well as the corresponding parasitic U. esculenta. Twelve microsatellites markers were used to study the genetic variations of 32 wild populations and 135 landraces of Z. latifolia. Model simulations based on approximate Bayesian computation (ABC) were then performed to hierarchically infer the population history. We also analyzed the ITS sequences of the smut fungus U. esculenta to reveal its genetic structure. Our results indicated a significant genetic divergence between cultivated Z. latifolia and its wild ancestors. The wild Z. latifolia populations showed significant hierarchical genetic subdivisions, which may be attributed to the joint effect of isolation by distance and hydrological unconnectedness between watersheds. Cultivated Z. latifolia was supposedly domesticated once in the low reaches of the Yangtze River. The genetic structure of U. esculenta also indicated a single domestication event, and the genetic variations in this fungus might be associated with the diversification of cultivars. These findings provided molecular evidence in accordance with the historical literature that addressed the domestication of cultivated Z. latifolia involved adaptive evolution driven by artificial selection in both the plant and fungus.

Keywords: Ustilago esculenta; Zizania latifolia; approximate Bayesian computation; domestication; genetic structure.

Figure 1

Geographical locations of 32 wild Zizania latifolia populations in China (red filled circles).

Figure 2

Genetic structure in Zizania latifolia. (A) The genetic divergence between wild populations and landraces was illustrated by STRUCTURE (K = 2). (B) Principal Coordinate Analysis (PCoA) of 32 wild populations and cultivated accessions. (C) The estimations of ΔK. (D) Genetic subdivisions in the wild populations of Z. latifolia (when K = 3, 5 and 6).

Figure 3

Genetic structure and settings of two competing scenarios in the wild Zizania latifolia populations. (A) Genetic structure of wild populations illustrated by STRUCTURE. Each vertical bar represents an individual, and each color represents a cluster in the histograms of STRUCTURE. (B) Two competing scenarios for ABC simulations. CLT is the cultivated group, South is the south group, and North is the north group. These groups were assumed to be isolated from each other, with no exchange of migrants. In Scenario A (SA), the southern group was separated from the northern group at time scale t2, with no changes in effective population size; at time scale t1, the cultivated group was then separated from the southern group and went through a bottleneck with an effective population size change from Ns to N1.

Figure 4

Genetic structure and settings of nine competing scenarios in the southern genetic group of wild Zizania latifolia. (A) The subtle genetic structure in the southern genetic group of Z. latifolia revealed by STRUCTURE. Each vertical bar represents an individual, and each color represents a cluster in the histograms of STRUCTURE. (B) 9 competing scenarios for ABC simulations inferring the origin of cultivars in the south group of wild Z. latifolia populations. CLT is the cultivated group, Pop1 is the Hongze-Tai lake group, Pop2 is the Poyang lake group, and Pop4 is the Dongting lake group.

Figure 5

Phylogeny tree (maximum parsimony, MP) for the 37 accessions (wild accessions in green and cultivated accessions in cyan) of Ustilago esculenta, Ustilago alcornii is the outgroup (in red). Bootstrap values calculated over 1,000 replications are given as percentages (only values > 50% were shown).