Abstract
To investigate the genetic and molecular regulation that the female gametophyte could exert over neighboring sporophytic regions of the ovule, we performed a quantitative comparison of global expression in wild-type and nozzle/sporocyteless (spl) ovules of Arabidopsis thaliana (Arabidopsis), using Massively Parallel Signature Sequencing (MPSS). This comparison resulted in 1517 genes showing at least 3-fold increased expression in ovules lacking a female gametophyte, including those encoding 89 transcription factors, 50 kinases, 25 proteins containing a RNA-recognition motif (RRM), and 20 WD40 repeat proteins. We confirmed that eleven of these genes are either preferentially expressed or exclusive of spl ovules lacking a female gametophyte as compared to wild-type, and showed that six are also upregulated in determinant infertile1 (dif1), a meiotic mutant affected in a REC8-like cohesin that is also devoided of female gametophytes. The sporophytic misexpression of IOREMPTE, a WD40/transducin repeat gene that is preferentially expressed in the L1 layer of spl ovules, caused the arrest of female gametogenesis after differentiation of a functional megaspore. Our results show that in Arabidopsis, the sporophytic-gametophytic cross talk includes a negative regulation of the female gametophyte over specific genes that are detrimental for its growth and development, demonstrating its potential to exert a repressive control over neighboring regions in the ovule.
Highlights
The ovules of flowering plants are most often formed as elongated primordia emerging from the inner surface of the young carpel, with the integument mounds initiating from periclinal divisions of the epidermal layer [1,2,3,4]
A large body of molecular, genetic and physiological evidence indicates that growth and development of the diploid sporophytic tissues of the ovule are fundamental for female gametogenesis, double fertilization and seed formation [1,19,20,21,49,50]
We took advantage of Massively Parallel Signature Sequencing (MPSS)-based large-scale transcriptional comparisons to identify 1,517 genes that are upregulated in spl ovules lacking female gametophyte as compared to wild-type
Summary
The ovules of flowering plants are most often formed as elongated primordia emerging from the inner surface of the young carpel, with the integument mounds initiating from periclinal divisions of the epidermal layer [1,2,3,4]. The integuments grow to progressively envelop the nucellus; by converging at the apex of the differentiated ovule, they form the micropyle, an extracellular narrow canal through which a pollen tube reaches the female gametophyte to deliver the sperm cells during double fertilization [5]. In Arabidopsis thaliana, the megaspore mother cell (MMC) differentiates sub-epidermally, and undergoes meiosis to differentiate a single functional megaspore that divides mitotically to form a female gametophyte composed of the egg cell, two synergids, three antipodals at the chalazal region, and a binucleated central cell whose nuclei fuse prior to fertilization. The egg cell and the central cell give rise to the embryo and the endosperm respectively; while the function of synergids is to attract the pollen tube, the function of the antipodals remains unknown
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