Transcriptome atlas of the Arabidopsis funiculus – a study of maternal seed subregions

Abstract

These authors contributed equally to this manuscript. SUMMARYThe funiculus anchors the structurally complex seed to the maternal plant, and is the only direct route of transport for nutrients and maternal signals to the seed. While our understanding of seed development is becoming clearer, current understanding of the genetics and cellular mechanisms that contribute to funiculus development is limited. Using laser microdissection combined with global RNA-profiling experiments we compared the genetic profiles of all maternal and zygotic regions and subregions during seed development. We found that the funiculus is a dynamic region of the seed that is enriched for mRNAs associated with hormone metabolism, molecular transport, and metabolic activities corresponding to biological processes that have yet to be described in this maternal seed structure. We complemented our genetic data with a complete histological analysis of the funiculus from the earliest stages of development through to seed maturation at the light and electron microscopy levels. The anatomy revealed signs of photosynthesis, the endomembrane system, cellular respiration, and transport within the funiculus, all of which supported data from the transcriptional analysis. Finally, we studied the transcriptional programming of the funiculus compared to other seed subregions throughout seed development. Using newly designed in silico algorithms, we identified a number of transcriptional networks hypothesized to be responsible for biological processes like auxin response and glucosinolate biosynthesis found specifically within the funiculus. Taken together, patterns of gene activity and histological observations reveal putative functions of the understudied funiculus region and identify predictive transcriptional circuits underlying these biological processes in space and time.

Nutritional functions of the funiculus in Brassica napus seed maturation revealed by transcriptome and dynamic metabolite profile analyses

“…Sucrose may be directly transported into seeds by sucrose transporters (SUT) (Weise et al 2000; Sauer 2007), without needing to be turned over into other forms, resulting in a linear correlation between sucrose and seed weight. A previous microarray study showed that AtSUT4 is highly expressed in the Arabidopsis funiculus (Khan et al 2015) and in our transcriptome data, BnSUT1, BnSUT4, BnSUT5, BnSUT6 , and other carbohydrate transporter genes BnGTP1, BnUTR2, BnPMT5, BnVGT1, BnPLT5 and BnPLT2 were also active in the B. napus funiculus (Fig. 6a).…”

“…1g) showed that the funiculus was ready to service the seed at a structural level. Previous histology studies revealed that the funiculi of B. napus (Chan and Belmonte 2013; Millar et al 2015), Arabidopsis (Belmonte et al 2013; Khan et al 2015), and Phaseolus vulgaris (Mawson et al 1994) showed proliferation of the vasculature tissue from the ovule to the globular stage, supporting transport as a primary function during seed filling. During the development of B. napus seed, the seed fresh weight increased nearly twofold during the morphogenesis phase from 7 to 21 DAF, and then continuously increased during seed filling from 21 to 35 DAF (Fig.…”

“…Morphological and histological observations showed that development of the funiculus occurs dynamically with seed development. Indeed, changes in the structural organization of the funiculus are necessary for normal seed growth, especially for its role in transport of nutrients into the seed (Mawson et al 1994; Chan and Belmonte 2013; Khan et al 2015; Millar et al 2015). From the ovule to the globular stage of seed development, the vascular strand (particularly the phloem) becomes much larger by increasing the number of cells of the vasculature.…”

“…Comprehensive molecular analysis of the distal seed coat (SC) and the chalazal seed coat (CZSC) of Arabidopsis thaliana and Brassica napus revealed that specific populations of mRNAs accumulated specifically in the CZSC and not in other seed regions (Belmonte et al 2013; Khan et al 2015; Millar et al 2015). A systems biology approach that compared the transcriptome of the funiculus to the transcriptomes of the SC and CZSC in both space and time revealed profound differences in the molecular machinery controlling adjacent seed coat sub-regions at the transcriptional level.…”

“…A systems biology approach that compared the transcriptome of the funiculus to the transcriptomes of the SC and CZSC in both space and time revealed profound differences in the molecular machinery controlling adjacent seed coat sub-regions at the transcriptional level. This comparison showed that transcripts involved in the transport and metabolism of sugar, amino acids, lipids, and hormonal regulation are expressed in the funiculus at specific stages of seed development that coincide with the timing of integral processes associated with embryonic growth and the accumulation of oil and protein (Khan et al 2015). These results provide a putative molecular basis for understanding the development of the funiculus; however, these activated genes involved in various metabolic pathways remain poorly understood, although they likely have important functions in supply and transport of nutrients demanded by seed filling, thereby controlling the quantity and the quality of seed storage reserves.…”