How exposure to ALS-inhibiting gametocide tribenuron-methyl induces male sterility in rapeseed

Jing-long Lian,Cheng-Yu Yu,Li-Suo Ren,Cong Zhang,Ai-Xia Xu,Zhen Huang,Jun-Gang Dong

doi:10.1186/s12870-019-1722-1

Jing-long Lian, Cheng-Yu Yu + Show 5 more

Open Access

https://doi.org/10.1186/s12870-019-1722-1

Copy DOI

Abstract

BackgroundAcetolactate synthase (ALS)-inhibiting herbicide tribenuron-methyl (TBM) is an efficient gametocide that can cause rapeseed (Brassica napus L.) to become male sterile and outcrossing. To find the reason the TBM treatment leads to male sterility, an integrated study using cytological, physiological, and transcriptomic methods was conducted.ResultsSome temporary symptoms, including the discoloration of young leaves and a short halt of raceme elongation, were observed in the rapeseed plants exposed to TBM at an application rate of 1 μg per plant. Both chloroplasts in young leaves and plastids in anthers were deformed. TBM also reduced the leaf photosynthetic rate and the contents of chlorophyll, soluble sugar and pyruvate. Both the tapetal cells and uni-nucleate microspores in the treated plants showed large autophagic vacuoles, and the tissue degenerated quickly. A transcriptomic comparison with the control identified 200 upregulated and 163 downregulated differential expression genes in the small flower buds of the TBM treatment. The genes encoding functionally important proteins, including glucan endo-1,3-beta-glucosidase A6, QUARTET3 (QRT3), ARABIDOPSIS ANTHER 7 (ATA7), non-specific lipid-transfer protein LTP11 and LTP12, histone-lysine N-methyltransferase ATXR6, spermidine coumaroyl-CoA acyltransferase (SCT), and photosystem II reaction centre protein psbB, were downregulated by TBM exposure. Some important genes encoding autophagy-related protein ATG8a and metabolic detoxification related proteins, including DTX1, DTX6, DTX35, cytosolic sulfotransferase SOT12, and six members of glutathione S-transferase, were upregulated. In addition, several genes related to hormone stimulus, such as 1-aminocyclopropane-1-carboxylate synthase 8 (ACS8), ethylene-responsive factor ERF1A, ERF1, ERF71, CRF6, and RAP2-3, were also upregulated. The transcriptional regulation is in accordance with the functional abnormalities of pollen wall formation, lipid metabolism, chloroplast structure, ethylene generation, cell cycle, and tissue autophagy.ConclusionThe results suggested that except for ALS, the metabolic pathways related to lipid metabolism, pollen exine formation, photosynthesis and hormone response are associated with male sterility induced by TBM. The results provide new insight into the molecular mechanisms of inducing male sterility by sulfonylurea.

Highlights

Acetolactate synthase (ALS)-inhibiting herbicide tribenuron-methyl (TBM) is an efficient gametocide that can cause rapeseed (Brassica napus L.) to become male sterile and outcrossing
In addition to the male sterility (MS) phenotype, TBM had some morphological influences on rapeseed, including the temporary depression of the stem elongation and discoloration of young leaves in the first several days, indicating a phytotoxic effect on cell growth, chloroplast structure, and/or flavonoid biosynthesis
To offset the metabolic detoxification during the long period of flowering that can last for three weeks, TBM exposure of a higher dose was used to prolong the gametocidal effect on the anther

Summary

Introduction

Acetolactate synthase (ALS)-inhibiting herbicide tribenuron-methyl (TBM) is an efficient gametocide that can cause rapeseed (Brassica napus L.) to become male sterile and outcrossing. Except for the herbicidal activity of ALS-inhibitors, many members of SU and the imidazolinone family, for example, tribenuron-methyl (TBM), amidosulfuron, and imazethapyr (IM), were identified to be good gametocides that can induce complete male sterility (MS) in many cruciferous species or some cereal plants when applied at sub-lethal amounts [3,4,5,6,7,8,9,10]. This MS belongs to chemically induced MS (CIMS). Breeding based on CIMS has had great success in China, and more than 20 commercial hybrid rapeseed (Brassica napus L.) varieties based on CIMS have been registered [10]

Objectives

Methods

Results

Discussion

Conclusion