Genome balance and dosage effect drive allopolyploid formation in Brassica

Author:

Cao Yao12ORCID,Zhao Kanglu12ORCID,Xu Junxiong12ORCID,Wu Lei12,Hao Fangyuan12,Sun Meiping12,Dong Jing12,Chao Getu12,Zhang Hong12,Gong Xiufeng12,Chen Yangui3,Chen Chunli45,Qian Wei3,Pires J. Chris6,Edger Patrick P.78,Xiong Zhiyong12

Affiliation:

1. Key Laboratory of Herbage and Endemic Crop Biology, Ministry of Education, Inner Mongolia University, Hohhot, Inner Mongolia 010070, China

2. College of Life Science, Inner Mongolia University, Hohhot, Inner Mongolia 010070, China

3. College of Agronomy and Biotechnology, Southwest University, Chongqing 400715, China

4. College of Life Science and Technology, Huazhong Agricultural University, Wuhan 430070, China

5. Key Laboratory of Plant Resource Conservation and Germplasm Innovation in Mountainous Region (Ministry of Education), College of Life Science, Guizhou University, Guiyang 550025, China

6. Department of Soil and Crop Sciences, Colorado State University, Fort Collins, CO 80523

7. Department of Horticulture, Michigan State University, East Lansing, MI 48823

8. Genetics and Genome Sciences Program, Michigan State University, East Lansing, MI 48824

Abstract

Polyploidy is a major evolutionary force that has shaped plant diversity. However, the various pathways toward polyploid formation and interploidy gene flow remain poorly understood. Here, we demonstrated that the immediate progeny of allotriploid AAC Brassica (obtained by crossing allotetraploid Brassica napus and diploid Brassica rapa ) was predominantly aneuploids with ploidal levels ranging from near-triploidy to near-hexaploidy, and their chromosome numbers deviated from the theoretical distribution toward increasing chromosome numbers, suggesting that they underwent selection. Karyotype and phenotype analyses showed that aneuploid individuals containing fewer imbalanced chromosomes had higher viability and fertility. Within three generations of self-fertilization, allotriploids mainly developed into near or complete allotetraploids similar to B. napus via gradually increasing chromosome numbers and fertility, suggesting that allotriploids could act as a bridge in polyploid formation, with aneuploids as intermediates. Self-fertilized interploidy hybrids ultimately generated new allopolyploids carrying different chromosome combinations, which may create a reproductive barrier preventing allotetraploidy back to diploidy and promote gene flow from diploids to allotetraploids. These results suggest that the maintenance of a proper genome balance and dosage drove the recurrent conversion of allotriploids to allotetraploids, which may contribute to the formation and evolution of polyploids.

Funder

the National Natural Science Foundation of China

the USA National Science Foundation

USDA-NIFA Hatch

Publisher

Proceedings of the National Academy of Sciences

Subject

Multidisciplinary

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