Identification of key regulatory genes involved in the sporophyte and gametophyte development in Ginkgo biloba ovules revealed by in situ expression analyses

Abstract

Premise In Arabidopsis thaliana, the role of the most important key genes that regulate ovule development is widely known. In nonmodel species, and especially in gymnosperms, the ovule developmental processes are still quite obscure. In this study, we describe the putative roles of Ginkgo biloba orthologs of regulatory genes during ovule development. Specifically, we studied AGAMOUS (AG), AGAMOUS‐like 6 (AGL6), AINTEGUMENTA (ANT), BELL1 (BEL1), Class III HD‐Zip, and YABBY Ginkgo genes. Methods We analyzed their expression domains through in situ hybridizations on two stages of ovule development: the very early stage that corresponds to the ovule primordium, still within wintering buds, and the late stage at pollination time. Results GBM5 (Ginkgo ortholog of AG), GbMADS8 (ortholog of AGL6) and GbC3HDZ1‐2‐3 were expressed in both the stages of ovule development, while GbMADS1, GbAGL6‐like genes (orthologs of AGL6), GbBEL1‐2 and YABBY Ginkgo orthologs (GbiYAB1B and GbiYABC) seem mostly involved at pollination time. GbANTL1 was not expressed in the studied stages and was different from GbANTL2 and GbBEL1, which seem to be involved at both stages of ovule development. In Ginkgo, the investigated genes display patterns of expression only partially comparable to those of other studied seed plants. Conclusions The expression of most of these regulatory genes in the female gametophyte region at pollination time leads to suggest a communication between the sporophytic maternal tissue and the developing female gametophyte, as demonstrated for well‐studied model angiosperms.

Does integument arise de novo or from pre-existing structures? ── Insights from the key regulatory genes controlling integument development

“…Gene expression analyses have clearly shown the expression of the ANT/AIL homologs in developing integuments in G. biloba (Wang et al, 2016;D'Apice et al, 2022), the conifer Pinus thunbergii (Shigyo and Ito, 2004;Yamada et al, 2008) and different species of Gnetum (Yamada et al, 2008;. Larsson et al and Schlögl et al showed the roles of the CUC homologs in regulating the differentiation of the shoot apical meristem (SAM) and embryogenesis in Picea abies (Larsson et al, 2012) and Araucaria angustifolia (Schlogl et al, 2012), respectively, as consistent with the roles in Arabidopsis (Chakraborty and Roy, 2019).…”

“…Larsson et al and Schlögl et al showed the roles of the CUC homologs in regulating the differentiation of the shoot apical meristem (SAM) and embryogenesis in Picea abies (Larsson et al, 2012) and Araucaria angustifolia (Schlogl et al, 2012), respectively, as consistent with the roles in Arabidopsis (Chakraborty and Roy, 2019). A strong expression of the BEL1 homolog has been detected in the integument in G. biloba D'Apice et al, 2022). The homologs of C3HDZ and ATS/KAN were expressed throughout ovule development in G. biloba D'Apice et al, 2022) and the Gnetum species (Zumajo-Cardona and Ambrose, 2021).…”

“…A strong expression of the BEL1 homolog has been detected in the integument in G. biloba D'Apice et al, 2022). The homologs of C3HDZ and ATS/KAN were expressed throughout ovule development in G. biloba D'Apice et al, 2022) and the Gnetum species (Zumajo-Cardona and Ambrose, 2021). The INO/YAB homologs were also found to be expressed in the ovule integument in Ephedra distachya (Finet et al, 2016).…”

All together now: Cellular and molecular aspects of leaf development in lycophytes, ferns, and seed plants

“…Correlation between expression of the genes encoding adaxial/abaxial determinants and the leaf anatomy is ambiguous: in leaves of Abies holophylla composed of palisade and spongy mesophyll and in Picea smithiana with only spongy and no palisade mesophyll, an ARP homolog is expressed in a stripe between leaf margins (Du et al, 2020). YABBY expression marks entire young leaves of Pseudotsuga menziesii, A. holophylla, and P. smithiana (Du et al, 2020) despite their anatomical differences, but is confined to the abaxial leaf domain in G. biloba (Finet et al, 2016;D'Apice et al, 2022). Thus ARP, C3HDZ, YABBY and KANADI TFs did not gain the strict role in control of development of the ad/abaxial leaf domains in gymnosperms (Du et al, 2018(Du et al, , 2020.…”

Sucrose promotes cone enlargement via the TgNGA1‐TgWRKY47‐TgEXPA2 module in Torreya grandis

“…After fertilization, the cone either enters a dormant state or undergoes rapid enlargement, which is crucial for seed production, plant reproduction, and seed yield in gymnosperms (Friedman, 2015;Kuhn et al, 2023). Despite its importance, our knowledge of cone development over the past century has largely been confined to gametophyte development and changes in anatomical structures observed in various species, including Ginkgo biloba, Araucaria angustifolia, and others (Florin, 1951;Owens & Moulder, 1977;Owens, 1984;Friedman, 2015;D'Apice et al, 2022;Elgorriaga & Atkinson, 2023;Kuhn et al, 2023). Over the past few years, the roles of several proteins potentially involved in cone development have been identified, including MADS-box, AGAMOUS-LIKE6, and CONSTANS-like proteins (Carlsbecker et al, 2013;Wang et al, 2020Wang et al, , 2022Yang et al, 2024).…”