The regulatory role of CARBON STARVED ANTHER-mediated photoperiod-dependent male fertility in rice

Abstract

Environmental signals, especially daylength, play important roles in determining fertility in photoperiod-sensitive genic male sterile (PGMS) lines that are critical to sustain production of high-yielding hybrid rice (Oryza sativa) varieties. However, the mechanisms by which PGMS lines perceive changes in photoperiod and transmit those signals to elicit downstream effects is not well understood. In this study, we compared the transcriptomes from the leaves and anthers of carbon starved anther (csa), a PGMS line, to wild-type tissues under different photoperiods. Components of circadian clock in the leaves, including Circadian Clock-Associated 1 (CCA1) and Pseudo-Response Regulator (PRR95), played vital roles in sensing the photoperiod signals. Photoperiod signals were weakly transduced to anthers, where gene expression was mainly controlled by the CSA allele. CSA played a critical role in regulating sugar metabolism and cell wall synthesis in anthers under short-day conditions, and transcription of key genes inducing csa-directed sterility was up-regulated under long-day (LD) conditions though not to wild-type levels, revealing a mechanism to explain the partial restoration of fertility in rice under LD conditions. Eight direct targets of CSA regulation were identified, all of which were genes involved in sugar metabolism and transport (cell wall invertases, SWEETs, and monosaccharide transporters) expressed only in reproductive tissues. Several hub genes coordinating the effects of CSA regulation were identified as critical elements determining wild-type male fertility, and further analysis of these and related genes will reveal insights into how CSA coordinates sugar metabolism, cell wall biosynthesis, and photoperiod sensing in rice anther development.

Source-To-Sink Transport of Sugar and Its Role in Male Reproductive Development

“…Rice DNA BINDING WITH ONE FINGER 11 (OsDOF11) modulates sugar transport by regulating the expression of several sugar transporter genes, including OsSUT1 , OsSUT3 , OsSUT4 , OsSUT5 , OsSWEET11 and OsSWEET14 , and its mutant has defects in plant height and panicle development ( Figure 3 ) [ 107 ]. Carbon Starved Anther (CSA) is reported to be a R2R3 MYB transcription factor regulating sugar transport during anther development, and also regulates OsSWEET14 expression ( Figure 3 ) [ 11 , 44 ]. The csa mutant reveals a photoperiod-sensitive genic male sterile phenotype due to the disruption of sugar supply to the anther under different photoperiods: male-sterile under short-day conditions but only semi-sterile under long-day conditions [ 11 , 12 ].…”

“…Interestingly, CSA2, another MYB transcription factor, reveals the reverse phenotypes, being fertile under short-day and semi-sterile under long-day conditions [ 13 ]. A further study suggests that CSA2 shares common downstream genes involved in sugar metabolism with CSA including OsSWEET6a , OsINV4 , OsAZT3 , OsSPT17 , and OsSPT27 ( Figure 3 ) [ 13 , 44 ].…”

“…CSA has a higher expression level in rice anthers under short-day conditions than long-day conditions, while the expression of CSA2 reveals the opposite variations under different day-length conditions [ 12 , 13 ]. Transcriptome data reveal that core components of the circadian clock, CCA1 and PRR95 , play vital roles in sensing the photoperiod signals, and are then transduced to anthers [ 13 , 44 ]. CSA and CSA2 are likely to be regulated by these photoperiod signals, then control the source-to-sink transport via downstream sugar transporters to influence anther development ( Figure 3 ) [ 13 , 44 ].…”

“…Transcriptome data reveal that core components of the circadian clock, CCA1 and PRR95 , play vital roles in sensing the photoperiod signals, and are then transduced to anthers [ 13 , 44 ]. CSA and CSA2 are likely to be regulated by these photoperiod signals, then control the source-to-sink transport via downstream sugar transporters to influence anther development ( Figure 3 ) [ 13 , 44 ]. These results suggest the importance of these transcription factors in sensing environmental signals and regulating normal growth, especially anther development.…”

Homology-based identification of candidate genes for male sterility editing in upland cotton (Gossypium hirsutum L.)

“…Formation of the tapetum is a critical part of anther development, as the tapetum will collect resources from vascular tissue to redistribute to developing microspores ( Pacini, 2010 ). Premature cell death of tapetal cells prevents the viability of pollen cells and is controlled by a variety of genes including Baymax1 , Carbon Starved Anther , Aborted Microspores , and AtMs1 ( Sorensen et al., 2003 ; Zhang et al., 2010 ; Zhang et al., 2013 ; Li et al., 2016 ; Zhang et al., 2018 ; An et al., 2020 ; Xiang et al., 2021 ; Li et al., 2022 ). Traditionally, anther development is divided into 10 stages with meiosis occurring in stage 1 and 2, followed by mitotic divisions to form tetrads in stages 3-4.…”