Progressive programmed cell death inwards across the anther wall in male sterile flowers of the gynodioecious plant Plantago lanceolata

Abstract

Main conclusion A cell death signal is perceived and responded to by epidermal cells first before being conveyed inwards across the anther wall in male sterile Plantago lanceolata flowers.In gynodioecious plants, floral phenotype is determined by an interplay between cytoplasmic male sterility (CMS)-promoting factors and fertility-restoring genes segregating in the nuclear background. Plantago lanceolata exhibits at least four different sterilizing cytoplasms. MS1, a "brown-anther" male sterile phenotype, segregates with a CMSI cytoplasm and a non-restoring nuclear background in P. lanceolata populations. The aim of this study was to investigate the cytology of early anther development in segregating hermaphrodite and male sterile flowers sharing the same CMSI cytoplasm, and to determine if the sterility phenotype correlates with any changes to the normal pattern of programmed cell death (PCD) that occurs during anther development. Cytology shows cellular abnormalities in all four anther wall layers (epidermis, endothecium, middle layer and tapetum), the persistence and enlargement of middle layer and tapetal cells, and the failure of microspore mother cells to complete meiosis in male sterile anthers. In these anthers, apoptotic-PCD occurs earlier than in fertile anthers and is detected in all four cell layers of the anther wall before the middle layer and tapetal cells become enlarged. PCD is separated spatially and temporally within the anther wall, occurring first in epidermal cells before extending radially to cells in the inner anther wall layers. This is the first evidence of a cell death signal being perceived and responded to by epidermal cells first before being conveyed inwards across the anther wall in male sterile plants.

bHLH010/089 Transcription Factors Control Pollen Wall Development via Specific Transcriptional and Metabolic Networks in Arabidopsis thaliana

“…As the tapetum acts as a supplier of sporopollenin precursors for pollen exine development, the normal development and programmed cell death (PCD) of the tapetum are essential for pollen development, including pollen exine formation [ 5 ]. Either abnormal development or advanced/delayed PCD of a tapetum leads to impaired pollen wall development and reduced male fertility [ 53 , 54 , 55 , 56 , 57 , 58 , 59 , 60 , 61 , 62 , 63 , 64 , 65 ]. A genetic transcriptional pathway has been demonstrated to function in regulating the development and PCD of a tapetum, from the upstream to the downstream, including the following transcription factor (TF) genes: dysfunctional tapetum 1 ( DYT1 ), bHLH010/bHLH089/bHLH091 , defective in tapetal development and function 1 ( TDF1 )/ MYB35 , and aborted microspores ( AMS ), MYB103 [ 66 , 67 , 68 , 69 , 70 , 71 , 72 , 73 , 74 ].…”

MicroRNAs Involved in Regulatory Cytoplasmic Male Sterility by Analysis RNA-seq and Small RNA-seq in Soybean

“…Pollen cell wall development is a crucial part of pollen production, and an abnormal pollen cell wall may be associated with male sterility in plants ( Li et al, 2006 ; Ma et al, 2007 ; Wijeratne et al, 2007 ; Wei et al, 2013a ; Hu et al, 2016 ; Xu et al, 2017 ; Zhou et al, 2017 ; Chen et al, 2018 , 2019 ; Hamid et al, 2019 ; Nugent et al, 2019 ; Sutthinon et al, 2019 ; Mondol et al, 2020 ). Some genes controlling pollen development have been identified and cloned ( Shi et al, 2011 ), including DMD1 ( Ren et al, 2020 ), DPW2 ( Xu et al, 2017 ), and DPW3 ( Mondol et al, 2020 ).…”

Comparative Transcriptome Analysis Reveals the Potential Mechanism of Abortion in Tobacco sua-Cytoplasmic Male Sterility

“…PCD is an ordered process of the selective removal of cells, and it is essential for the growth and development of multicellular organisms, as well as for proper environmental responses [38]. Aberrant PCD is also the abortion mechanism of much CMS, mainly manifested by premature and delayed PCD of the tapetum in microsporogenesis or uninucleate stages [22,[39][40][41].…”