The genomic and transcriptomic foundations of viviparous seed development in mangroves

Abstract

Vivipary in plants refers to a specific seed development and reproductive strategy where seeds minimize the dormancy stage and germinate while still attached to their maternal plants. It is one of the most unique adaptive genetic features used by many mangrove species where elongated hypocotyls aid in quick root emergence to anchor the seedling in coastal intertidal wetlands. The genetic mechanisms behind mangrove vivipary, however, remain elusive. Using comparative genomic and transcriptomic technologies to investigate viviparous mangroves and their close inland relatives, we found that a full array of gene expression profiles were altered, including key plant hormone metabolic pathways, high expression of embryonic signature genes, and reduced production of proanthocyanidins and storage proteins. Along with these changes, a major gene regulating seed dormancy, Delay of Germination-1 (DOG1), is entirely missing or defunct within the entire linage of the four genera with true viviparous characteristics. These results suggest a systemic level change is required to warrant the genetic program of mangrove vivipary. Understanding of the molecular processes of vivipary could benefit the design of pregerminated propagules for forestation in harsh environments or prevent precocious germination of grain crops pre- and post-harvest.

Genetic and molecular mechanisms underlying mangrove adaptations to intertidal environments

“…Another K. obovata -specific transcription factor, ABI4, regulates primary seed dormancy by inhibiting the promoter activity of CYP707A . This provides a strong evidence for the relationship between repressed ABA signaling and lack of seed dormancy in mangroves ( Hong et al., 2018 ; Qiao et al., 2020 ). Differential gene expression analysis of A. officinalis reported upregulation of genes involved in ethylene and auxin signaling and down regulation of genes and transcription factors involved in ABA signaling such as MYBs , ABA-responsive element binding factors (ABFs) , and basic Leucine Zipper genes (bZIPs) ( Hong et al., 2018 ).…”

“…Vivipary is an adaptation facilitating dispersal and colonization of mangrove plants in hostile intertidal zones ( Qiao et al., 2020 ). In vivipary, the propagules germinate without dormancy period while attached to the parent tree ( Hong et al., 2018 ).…”

“…Because vivipary lacks dormancy period, the genes inducing dormancy are either lost or switched off to achieve this peculiar adaptation in mangroves. The Delay of germination 1 ( DOG1 ) gene which regulates seed dormancy is found to have lost in mangrove plants expressing true vivipary such as K. obovata , C. tagal , and R. apiculata ( Carrillo-Barral et al., 2020 ; Qiao et al., 2020 ). In contrast, the loss of heme-binding activity of the DOG1 gene in A. corniculatum might have resulted in the appearance of crypto vivipary ( Elmqvist and Cox, 1996 ; Feng et al., 2021 ).…”

“…Expression of proanthocyanidin (PA) synthetic enzymes, known to prevent seed germination, is also found to be lowered during vivipary in the embryos and seeds of K. obovata as well as C. brachiata . Among them, LAC15 and ANR genes having key roles in PA biosynthesis are more regulated in C. brachiata than K. obovata ( Qiao et al., 2020 ). The salient gene candidates with potential involvement in mangrove vivipary are summarized in Figure 4 .…”

A high-quality genome of the mangroveAegiceras corniculatumaids investigation of molecular adaptation to intertidal environments

“…Since DOG1 was first identified and cloned in A. thaliana as a major quantitative trait locus for seed dormancy (Bentsink et al, 2006), most mechanisms of seed dormancy have been elucidated in this species (Nonogaki, 2019). Recent genomic analyses in mangrove trees suggest that amino acid substitution and positive selection of essential seed development genes, expression changes of key plant hormone metabolism and embryonic genes, reduction of proanthocyanidin and storage protein production, and DOG1 loss together contribute to vivipary in the Rhizophoraceae family (Qiao et al, 2020;Xu et al, 2017). In the crypto-viviparous mangrove A. corniculatum embryos only break out of the seed coat before dehiscence.…”