Comparative analysis of wild‐type accessions reveals novel determinants of Arabidopsis seed longevity

Abstract

Understanding the genetic factors involved in seed longevity is of paramount importance in agricultural and ecological contexts. The polygenic nature of this trait suggests that many of them remain undiscovered. Here, we exploited the contrasting seed longevity found amongst Arabidopsis thaliana accessions to further understand this phenomenon. Concentrations of glutathione were higher in longer‐lived than shorter‐lived accessions, supporting that redox poise plays a prominent role in seed longevity. However, high seed permeability, normally associated with shorter longevity, is also present in long‐lived accessions. Dry seed transcriptome analysis indicated that the contribution to longevity of stored messenger RNA (mRNAs) is complex, including mainly accession‐specific mechanisms. The detrimental effect on longevity caused by other factors may be counterbalanced by higher levels of specific mRNAs stored in dry seeds, for instance those of heat‐shock proteins. Indeed, loss‐of‐function mutant analysis demonstrated that heat‐shock factors HSF1A and 1B contributed to longevity. Furthermore, mutants of the stress‐granule zinc‐finger protein TZF9 or the spliceosome subunits MOS4 or MAC3A/MAC3B, extended seed longevity, positioning RNA as a novel player in the regulation of seed viability. mRNAs of proteins with putative relevance to longevity were also abundant in shorter‐lived accessions, reinforcing the idea that resistance to ageing is determined by multiple factors.

Seed longevity and genome damage

“…Imbibed aged Arabidopsis seeds displayed stress responses associated with heat shock and increased expression of genes involved in RNA metabolism [ 91 ]. Consistent with these findings, long-lived Arabidopsis ecotypes display elevated transcript levels of heat shock factors and RNA processing genes, with the corresponding mutant lines displaying altered sensitivity to ageing [ 41 ]. An earlier study reported increased expression of Glutathione S Transferase U22 in dry aged seeds, potentially resulting from increased oxidative stress [ 92 ].…”

“…Seed ageing across a wide range of species and ageing regimes results in an elevated GSSG/2GSH ratio, indicative of increasingly oxidising values as seed lots lose viability [ 36–40 ]. This link between ageing and redox state is supported by the observation that Arabidopsis ecotypes with higher levels of glutathione display increased seed longevity [ 41 ]. The importance of redox homeostasis is supported by a Genome-Wide Association Study (GWAS) of 270 Arabidopsis ecotypes that identified several genes linked to increased longevity, including DEHYDROASCORBATE REDUCTASE 1 ( DHAR1 ) [ 42 ].…”

Genome-Wide Analysis and Expression Profiling of Glutathione Reductase Gene Family in Oat (Avena sativa) Indicate Their Responses to Abiotic Stress during Seed Imbibition

“…It is indispensable for the earliest metabolic events during seed germination and maintenance of seed vigor [ 14 ]. The level of GSH was suggested to be a promising indicator for seed germination and seedling growth, and was correlated with seed longevity [ 33 , 34 ]. GR is considered to be a crucial enzyme that works on the catalytic reduction of GSSG to the reduced GSH form, thereby involving in plant stress resistance, seed vigor maintenance, growth, and development.…”

Comparative Seeds Storage Transcriptome Analysis of Astronium fraxinifolium Schott, a Threatened Tree Species from Brazil

“…Seeds of different species and cultivars, preserved in germplasm banks under the same conditions of temperature and humidity, present different responses regarding the loss of viability [1]. This longevity is affected by several factors such as the chemical composition of the seed, maturation stage, initial viability, humidity, temperature and degree of infection by microorganisms and insects [10][11][12][13]. One of the main challenges to keep seed viability in germplasm banks is to predict when the accessions should be regenerated and to detect the initial stages of seed deterioration without consuming the samples in repetitive trials to evaluate the viability in the monitoring process [4].…”

“…Thus, several studies have analyzed the gene expression profile with a focus on development in order to identify possible genes responsible for the aging process in order to detect the beginning of the decline in seed viability [9,23,24]. Furthermore, the amount of mRNA present between short-lived and long-lived seed accessions, in addition to different associated processes, such as the presence of more heat-shock proteins in long-lived seed accessions, demonstrates that the interactions between genes are complex and determined by many factors [13].…”