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Deficiencies in the formation and regulation of anther cuticle and tryphine contribute to male sterility in cotton PGMS line.

ABSTRACT: BACKGROUND:Male sterility is a simple and efficient pollination control system that is widely exploited in hybrid breeding. In upland cotton, CCRI9106, a photosensitive genetic male sterile (PGMS) mutant isolated from CCRI040029, was reported of great advantages to cotton heterosis. However, little information concerning the male sterility of CCRI9106 is known. Here, comparative transcriptome analysis of CCRI9106 (the mutant, MT) and CCRI040029 (the wild type, WT) anthers in Anyang (long-day, male sterile condition to CCRI9106) was performed to reveal the potential male sterile mechanism of CCRI9106. RESULTS:Light and electron microscopy revealed that the male sterility phenotype of MT was mainly attributed to irregularly exine, lacking tryphine and immature anther cuticle. Based on the cytological characteristics of MT anthers, anther RNA libraries (18 in total) of tetrad (TTP), late uninucleate (lUNP) and binucleate (BNP) stages in MT and WT were constructed for transcriptomic analysis, therefore revealing a total of 870,4 differentially expressed genes (DEGs). By performing gene expression pattern analysis and protein-protein interaction (PPI) networks construction, we found down-regulation of DEGs, which enriched by the lipid biosynthetic process and the synthesis pathways of several types of secondary metabolites such as terpenoids, flavonoids and steroids, may crucial to the male sterility phenotype of MT, and resulting in the defects of anther cuticle and tryphine, even the irregularly exine. Furthermore, several lipid-related genes together with ABA-related genes and MYB transcription factors were identified as hub genes via weighted gene co-expression network analysis (WGCNA). Additionally, the ABA content of MT anthers was reduced across all stages when compared with WT anthers. At last, genes related to the formation of anther cuticle and tryphine could activated in MT under short-day condition. CONCLUSIONS:We propose that the down-regulation of genes related to the assembly of anther cuticle and tryphine may lead to the male sterile phenotype of MT, and MYB transcription factors together with ABA played key regulatory roles in these processes. The conversion of fertility in different photoperiods may closely relate to the functional expression of these genes. These findings contribute to elucidate the mechanism of male sterility in upland cotton.

SUBMITTER: Zhang M

PROVIDER: S-EPMC7685665 | biostudies-literature | 2020 Nov

REPOSITORIES: biostudies-literature

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Deficiencies in the formation and regulation of anther cuticle and tryphine contribute to male sterility in cotton PGMS line.

Zhang Meng M Liu Ji J Ma Qiang Q Qin Yuan Y Wang Hantao H Chen Pengyun P Ma Liang L Fu Xiaokang X Zhu Longfu L Wei Hengling H Yu Shuxun S

BMC genomics 20201123 1

<h4>Background</h4>Male sterility is a simple and efficient pollination control system that is widely exploited in hybrid breeding. In upland cotton, CCRI9106, a photosensitive genetic male sterile (PGMS) mutant isolated from CCRI040029, was reported of great advantages to cotton heterosis. However, little information concerning the male sterility of CCRI9106 is known. Here, comparative transcriptome analysis of CCRI9106 (the mutant, MT) and CCRI040029 (the wild type, WT) anthers in Anyang (long ...[more]

PMID: 33228563

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Project description:Genetic engineered male sterility has different applications, ranging from hybrid seed production to bioconfinement of transgenes in genetic modified crops. The impact of this technology is currently patent in a wide range of crops, including legumes, which has helped to deal with the challenges of global food security. Production of engineered male sterile plants by expression of a ribonuclease gene under the control of an anther- or pollen-specific promoter has proven to be an efficient way to generate pollen-free elite cultivars. In the last years, we have been studying the genetic control of flower development in legumes and several genes that are specifically expressed in a determinate floral organ were identified. Pisum sativum ENDOTHECIUM 1 (PsEND1) is a pea anther-specific gene displaying very early expression in the anther primordium cells. This expression pattern has been assessed in both model plants and crops (tomato, tobacco, oilseed rape, rice, wheat) using genetic constructs carrying the PsEND1 promoter fused to the uidA reporter gene. This promoter fused to the barnase gene produces full anther ablation at early developmental stages, preventing the production of mature pollen grains in all plant species tested. Additional effects produced by the early anther ablation in the PsEND1::barnase-barstar plants, with interesting biotechnological applications, have also been described, such as redirection of resources to increase vegetative growth, reduction of the need for deadheading to extend the flowering period, or elimination of pollen allergens in ornamental plants (Kalanchoe, Pelargonium). Moreover, early anther ablation in transgenic PsEND1::barnase-barstar tomato plants promotes the developing of the ovaries into parthenocarpic fruits due to the absence of signals generated during the fertilization process and can be considered an efficient tool to promote fruit set and to produce seedless fruits. In legumes, the production of new hybrid cultivars will contribute to enhance yield and productivity by exploiting the hybrid vigor generated. The PsEND1::barnase-barstar construct could be also useful to generate parental lines in hybrid breeding approaches to produce new cultivars in different legume species.

Project description:Male-sterile plants are used in hybrid breeding as well as for gene confinement for genetically modified plants in field trials and agricultural production. Apart from naturally occurring mutations leading to male sterility, biotechnology has added new possibilities for obtaining male-sterile plants, although so far only one system is used in practical breeding due to limitations in propagating male-sterile plants without segregations in the next generation or insufficient restoration of fertility when fruits or seeds are to be harvested from the hybrid varieties. Here a novel mechanism of restoration for male sterility is presented that has been achieved by interference with extracellular invertase activity, which is normally specifically expressed in the anthers to supply the developing microspores with carbohydrates. Microspores are symplastically isolated in the locular space of the anthers, and thus an unloading pathway of assimilates via the apoplasmic space is mandatory for proper development of pollen. Antisense repression of the anther-specific cell wall invertase or interference with invertase activity by expressing a proteinacious inhibitor under the control of the anther-specific invertase promoter results in a block during early stages of pollen development, thus causing male sterility without having any pleiotropic effects. Restoration of fertility was successfully achieved by substituting the down-regulated endogenous plant invertase activity by a yeast invertase fused to the N-terminal portion of potato-derived vacuolar protein proteinase II (PiII-ScSuc2), under control of the orthologous anther-specific invertase promoter Nin88 from tobacco. The chimeric fusion PiII-ScSuc2 is known to be N-glycosylated and efficiently secreted from plant cells, leading to its apoplastic location. Furthermore, the Nin88::PiII-ScSuc2 fusion does not show effects on pollen development in the wild-type background. Thus, such plants can be used as paternal parents of a hybrid variety, thereby the introgression of Nin88::PiII-ScSuc2 to the hybrid is obtained and fertility is restored. In order to broaden the applicability of this male sterility/restoration system to other plant species, a phylogenic analysis of plant invertases(beta-fructofuranosidases) and related genes of different species was carried out. This reveals a specific clustering of the cell wall invertases with anther-specific expression for dicotyl species and another cluster for monocotyl plants. Thus, in both groups of plants, there seems to be a kind of co-evolution, but no recent common ancestor of these members of the gene family. These findings provide a helpful orientation to classify corresponding candidate genes in further plant species, in addition to the species analysed so far (Arabidopsis, tobacco, tomato, potato, carrots, rice, and wheat).

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Deficiencies in the formation and regulation of anther cuticle and tryphine contribute to male sterility in cotton PGMS line.

Publications

Deficiencies in the formation and regulation of anther cuticle and tryphine contribute to male sterility in cotton PGMS line.

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