Compensation of Wild Plants Weakens the Effects of Crop-Wild Gene Flow on Wild Rice Populations.

Dongxin Ouyang,Ji Yang,Manqiu Xiao,Wenju Zhang,Shanshan Dong,Jianling You,Yao Zhao,Yuguo Wang,Zhiping Song

doi:10.3389/fpls.2021.681008

Abstract

Crop-wild gene flow may alter the fitness of the recipient i.e., crop-wild hybrids, then potentially impact wild populations, especially for the gene flow carrying selective advantageous crop alleles, such as transgenes conferring insect resistance. Given the continuous crop-wild gene flow since crop domestication and the occasionally stressful environments, the extant wild populations of most crops are still “wild.” One interpretation for this phenomenon is that wild populations have the mechanism buffered for the effects of crop alleles. However, solid evidence for this has been scarce. We used wild rice (Oryza rufipogon) and transgenic (Bt/CpTI) rice (O. sativa) as a crop-wild gene flow model and established cultivated, wild, and F7 hybrid rice populations under four levels of insect (Chilo suppressalis) pressure. Then, we measured the trait performance of the plants and estimated fitness to test the compensatory response of relatively high fitness compared to the level of insect damage. The performance of all plants varied with the insect pressure level; wild plants had higher insect-tolerance that was expressed as over- or equal-compensatory responses to insect damage, whereas crop and hybrids exhibited under-compensatory responses. The higher compensation resulted in a better performance of wild rice under insect pressure where transgenes conferring insect resistance had a somewhat beneficial effect. Remarkable hybrid vigour and the benefit effect of transgenes increased the fitness of hybrids together, but this joint effect was weakened by the compensation of wild plants. These results suggest that compensation to environmental stress may reduce the potential impacts of crop alleles on wild plants, thereby it is a mechanism maintaining the “wild” characteristics of wild populations under the scenario of continuous crop-wild gene flow.

Highlights

Crop-wild gene flow has occurred continuously since the domestication of crops, allowing crop alleles to introgress into wild populations (Ellstrand et al, 2013)
Few insects survived in the transgenic populations TP and KF8, while a large number of C. suppressalis occurred in the populations MH86, W, and TN (Figure 1A; Supplementary Table 2), in which the final insect density increased with the pressure level, but the rates of increase did not correspond with the initial gradient (χ2, p > 0.05)
The comparisons between hybrids and wild plants revealed that the hybrids had a taller plant height, much greater aboveground biomass, tillers, and seed yields, causing a higher relative fitness in the hybrids (FTN/W ) (Table 2; Supplementary Table 4) and indicating a hybrid vigour

Summary

Introduction

Crop-wild gene flow has occurred continuously since the domestication of crops, allowing crop alleles to introgress into wild populations (Ellstrand et al, 2013). A considerable proportion of the current O. rufipogon populations harbours domestication genes transferred from cultivated rice by gene flow (for instance, sh and PROG1 that are respectively responsible for two of the most critical domestication traits for rice: non-shattering grains and erect growth) (Wang et al, 2017), the wild rice populations still retain “wild” characteristics: typically displaying the traits of long awns, severe seed shattering, proanthocyanidin-pigmented pericarps, open panicles with few secondary branches bearing relatively few grains, and a nonerect to prostrate/creeping growth habit (Zheng et al, 2019) To explain this paradox, it is hypothesised that wild rice populations have evolved mechanisms to compensate the negative influence of crop gene flow on the seed bank and perennial habit of the wild population (Wang et al, 2017).

Methods

Results

Conclusion