Exposure to trace amounts of sulfonylurea herbicide tribenuron-methyl causes male sterility in 17 species or subspecies of cruciferous plants

Abstract

BackgroundFor most cruciferous plants, which are known as important crops and a number of weeds, hybrid breeding is hampered by the unavailability of a pollination control system. Male sterility induced by a gametocide can be useful for the utilization of plant heterosis.ResultsThe gametocidal effect of sulfonylurea herbicide tribenuron-methyl was tested across seventeen cruciferous species or subspecies including Brassica juncea, B. carinata, B. oleracea ssp. capitata, B. oleracea ssp. acephala, B. rapa ssp. pekinensis, B. rapa ssp. chinensis, B. rapa ssp. parachinensis, B. nigra, Orychophragmus violaceus, Matthiola incana, Raphanus sativa, Sisymbrium altissimum, Eruca sativa, Sinapis alba, Sinapis arvensis, Capsella bursa-pastoris and Camelina sativa. The plants of 23 cultivars in these species or subspecies were foliar sprayed with 10 ml of 0.2 or 0.4 mg/L of tribenuron-methyl before the vacuolated microspore formed in the largest flower buds; the application was repeated ten to twelve days afterwards. Tribenuron-methyl exposure significantly changed the flowering phenology and reproductive function. The treated plants demonstrated a one to four day delay in flowering time and a shortened duration of flowering, as well as other slight phytotoxic effects including a reduction in plant height and floral organ size. Approximately 80% to 100% male sterility, which was estimated by both pollen staining and selfing seed-set rate, was induced in the plants. As a result, plants were rendered functionally able to out-cross, with an average 87% and 54% manually pollinated seed-set rate compared to the corresponding controls at the 0.2 mg/L and 0.4 mg/L doses, respectively.ConclusionsThe results suggested that male reproductive function was much more sensitive to tribenuron-methyl exposure than female function. This sulfonylurea herbicide has a promising use as the gametocide for hybrid production in cruciferous plants.Electronic supplementary materialThe online version of this article (doi:10.1186/s12870-017-1019-1) contains supplementary material, which is available to authorized users.

Acetolactate Synthase-Inhibiting Gametocide Amidosulfuron Causes Chloroplast Destruction, Tissue Autophagy, and Elevation of Ethylene Release in Rapeseed

“…Some previous evidences suggested that valine, leucine and isoleucine may be involved in the regulation of cell division (Rost et al, 1990 ) and sulfonylurea herbicides disturbed cell division in the meristematic tissues of plants (Saja et al, 2016 ). We also found that amidosulfuron can restrain the raceme elongation (cell growth) in the first days after treatment and the pollen development was terminated before microspore mitosis (the flower bud length of 3–3.5 mm), as various sulfonylurea herbicides did in different cultivars (Yu et al, 2006 , 2009 , 2017 ; Yu and He, 2014 ; Li et al, 2015 ). The increase of endogenous ethylene in the treated plants may cause frustration on plant growth and development including cell cycle.…”

“…Nevertheless, obtention of highly efficient gametocides is the first task in a breeding scheme using CIMS. Some herbicides that inhibit acetolactate synthase (ALS; EC 4.1.3.18), such as tribenuron-methyl (Express) and amidosulfuron (Hoestar/Gratil), were showed to be able to induce complete male sterility in many cruciferous species when they were applied at trace amounts (about 1% dosage recommended for weed control; Yu et al, 2006 , 2009 , 2017 ; Yu and He, 2014 ; Li et al, 2015 ). In the last decade, over 20 commercial hybrid rapeseed varieties based on CIMS have been registered in China, for examples, Shaanyou1209, Zhongyouza19, Qinyou33, and Yuhuang1.…”

Male Sterility of an AHAS-Mutant Induced by Tribenuron-Methyl Solution Correlated With the Decrease of AHAS Activity in Brassica napus L.

“…Some chemicals have been reported as CHAs for hybrid seeds production in rapeseed ( Guan, 2014 ; Yu and He, 2014 ). A few of sulfonylurea herbicides, which are a class of the most widely used acetohydroxyacid synthase (AHAS, EC 2.2.1.6)-inhibiting herbicides, can induce complete male sterility in rapeseed at a concentration less than 1% of that required for their herbicide activity, such as tribenuron methyl (TBM) ( Yu et al, 2006 ; Zhang et al, 2010 ; Yu et al, 2017 ), monosulfuron-ester sodium ( Cheng et al, 2013 , 2015 ; Li Z. et al, 2015 ), and amidosulfuron ( Yu et al, 2009 ). So far, several dozens of commercial rapeseed ( B. napus ) hybrids based on male sterility induced by TBM or other sulfonylurea herbicides have been registered in China ( Cheng et al, 2013 ; Yu et al, 2017 ).…”

Sublethal application of various sulfonylurea and imidazolinone herbicides favors outcrossing and hybrid seed production in oilseed rape

“…It was found that the application of some sulfonylurea (SU) herbicides, such as tribenuron-methyl (TBM) [19] and amidosulfuron [20], had a strong gametocidal effect on OSR and allowed the treated plants to outcross. These SUs have been validated as useful gametocides for OSR and other Brassica species, and now, their different forms have been widely used by many institutes and seed companies in China [21]. More than 20 commercial hybrids based on SU gametocides have been released in China [21] by OSR breeders from Shaanxi, Hubei, Chongqing, Hunan, Sichuan, Jiangsu, Zhejiang, and Jiangxi provinces.…”

“…These SUs have been validated as useful gametocides for OSR and other Brassica species, and now, their different forms have been widely used by many institutes and seed companies in China [21]. More than 20 commercial hybrids based on SU gametocides have been released in China [21] by OSR breeders from Shaanxi, Hubei, Chongqing, Hunan, Sichuan, Jiangsu, Zhejiang, and Jiangxi provinces. SU herbicides target the acetolactate/acetohydroxylate synthase (ALS/ AHAS) enzyme, which is a key enzyme in the biosynthesis of valine, leucine, and isoleucine.…”