Transgenerational stress memory in seed and seedling vigor of peanut (Arachis hypogaea L.) varies by genotype

https://doi.org/10.1016/j.envexpbot.2019.03.006Get rights and content

Highlights

  • Water deficit during vegetative growth impacts seed vigor in peanut.

  • Two subspecies of peanut differ in when transgenerational stress memory manifests.

  • Transgenerational stress memory altered root architecture in two genotypes.

  • Phenotypes associated with stress memory cannot be generalized within species.

Abstract

Recent studies in plants and other organisms have suggested that ‘memories’ of stress events can be inherited from parent to offspring through a process known as transgenerational stress memory (TSM). However, TSM has not been adequately studied in many plant species, despite its potential role in stress adaptation. The objective of this study was to identify the effects of TSM on the development and vigor of peanut (Arachis hypogaea L.) seedlings of five genotypes. Seeds were collected from parents that received two water regimes representing contrasting TSM: 1) offspring from non-stressed parents and 2) offspring from stressed parents. Seed weight and vigor were tested using traditional methods, and both above- and belowground seedling vigor were analyzed using a rhizotron bioassay. There was a high variability between genotypes in how and when TSM was expressed, as illustrated by an interaction of offspring type and genotype in characteristics such as initial seed weight, germination, and rooting characteristics. These results contribute important documentation of the existence of TSM in plants and the need to further examine TSM capacity in plant adaptation to stress. Further, these results suggest that, for certain genotypes, water availability in the parent generation could be responsible for increased seed quality and vigor.

Introduction

As climate patterns shift in the southern region of the United States, rainfall patterns are becoming more variable and drought events are occurring more frequently and with greater severity (Kottapalli et al., 2009). Even in regions that previously received adequate rainfall to support optimal plant growth and performance, the increasing threat of water deficit is driving a need for a greater understanding of plant response and adaptation to stress. Notable progress has been made in advancing the understanding of crop responses under a variety of water deficit scenarios, in particular, largely in conjunction with the design of strategies for efficiently managing water-use and the identification of varieties that maintain performance during water scarcity (Cattivelli et al., 2008). However, even in plant species which have a wide knowledge base regarding stress response, there is significant potential for expansion of the study of adaptation to water deficit beyond the phenotypic expression of aboveground physiology under stress.

Recently, efforts to enhance drought adaptability have focused on short-term acclimation responses to water deficit within a single generation. These acclimation responses involve the capacity of plants to have a ‘stress memory’, whereby responses to stress events are altered with each repetition of stress exposure (e.g. Bruce et al., 2007; Walter et al., 2011). In crop plants, some management schemes are designed specifically to take advantage of these cisgenerational stress memories; for example, the primed acclimation management system that utilizes deficit irrigation during early plant development to induce physiological acclimation responses and harden plants to future stress (Rowland et al., 2012). Stress memories are hypothesized to be a mechanism that allows plants to rapidly adapt to local conditions (Boyko and Kovalchuk, 2011; Crisp et al., 2016) and may not only occur within a single individual’s lifetime, but across generations as well (Cullins, 1973; Shock et al., 1998; Monneveux et al., 2013). This type of environmentally induced parental effect has been reported for a number of organisms, including humans (Luppalainen and Greally, 2017) and plants (Iwasaki and Paszkowski, 2014), and is referred to as transgenerational stress memory (TSM). TSM is a phenotype resulting from the transmission of information from stress exposed parents to offspring and exceeding the direct action of both offspring genotype and environmental conditions (Lacy, 1998). That is, TSM represents those components of phenotypes expressed by offspring that are initiated by an environmental stimulus in the previous generation and cannot be completely explained by the parental genotype or immediate genotype by environment interaction.

TSM can play an integral role in forming the ultimate phenotype of a plant (Crews et al., 2012) and contribute to increased intergenerational physiological plasticity. By enabling stronger or more effective responses to environmental cues or stresses (Galloway, 2005; Walter et al., 2011; Asensi-Fabado et al., 2013; Munné-Bosch et al., 2013), TSM produces a wider range of seedling responses to the environment than would be possible through inherent offspring plasticity alone (Sultan et al., 2009). These responses allow for rapid adaptation to dynamic environments when the process of evolution through natural DNA mutation is too slow to enable adequate response to environmental perturbation (Boyko and Kovalchuk, 2011; Lim and Brunet, 2013; Heard and Martienssen, 2014). As a mechanism of inheritance of stress acclimation, TSM could be highly beneficial for sessile or short-lived, annual organisms like most crop plants (Grossniklaus et al., 2013; Lim and Brunet, 2013), ensuring the survival of some offspring regardless of whether the stressful conditions experienced by the parent are alleviated (Tricker, 2015; Bilichak and Kovalchuk, 2016). Adaptive effects have been observed in seedlings produced by drought-stressed parents of Polygonum persicaria, which have enhanced survival and competitive success in comparison to seedlings from well-watered parents (Sultan et al., 2009). Seedlings produced by parent plants exposed to stress by competition (Walter et al., 2016) and herbivory (Rasmann et al., 2012) also exhibit beneficial adaptations such as faster germination and increased stress resistance in comparison to offspring of parents not affected by stress. Unfortunately, TSM could also result in the inheritance of negative stress-related traits that either impair plant responses to current environmental conditions or reduce production (Iwasaki and Paszkowski, 2014) when there is mismatch between the offspring and parental environments.

In plants, the simplest form of TSM may involve maternal provisioning (Herman and Sultan, 2011; Crisp et al., 2016), which leads to alterations of the amount or composition of materials laid down within the seed during development. Epigenetics, including changes in gene expression induced by histone modification (Greer et al., 2011), chromatin remodeling (Bender, 2004), and DNA methylation (Henderson and Jacobson, 2007; Zilberman, 2008; Gonzalez et al., 2016), could also drive TSM (Kovalchuk, 2008; Crews et al., 2012; Eichten et al., 2014). It is also possible that combinations of mechanisms act in tandem to influence offspring phenotypes and create TSM (Herman and Sultan, 2011).

Indeed, some stresses or intensities of stress will result in epigenetic modification of phenotypes within and between generations, but other stresses or intensities of the same stress will not (Pecinka et al., 2010) because the driving mechanisms differ (Boyko et al., 2010). Many of the molecular mechanisms that induce transgenerational phenotype changes are also transient (Lang-Mladek et al., 2010; Tittel-Elmer et al., 2010). Therefore, the altered phenotype may be present in the absence of the epigenetic mark responsible. The opposite can be true, as well; van Dooren et al. (2018) observed changes in DNA methylation induced by mild drought in Arabidopsis, but no associated differences in gene expression or phenotype were detected. The current understanding of the dynamics of molecular mechanisms of TSM is based largely on studies conducted on Arabidopsis spp. that have a smaller, simpler genome than many crop species. But given the complexity and specificity of both the molecular and physiological mechanisms of TSM, caution should be exercised when comparing TSM between model and other plant species (Boyko and Kovalchuk, 2011). Identifying the exact mechanism of TSM in a given species will require in-depth knowledge of the physiological and morphological changes produced by TSM, when these changes occur in development, and their associated genetic background. Only with this information will it be possible to link epigenetic marks with their functional significance and validate those mechanisms (Richards et al., 2017). Thus, the first step in successful studies of epigenetic effects is extensive phenotyping of traits related to TSM.

A full understanding of drought tolerance and TSM must include phenotypic alterations that may impact the next generation. Knowledge of the relationship between TSM, seedling germination, vigor, and development in generations following stress events could be critical in elucidating the breadth of stress adaptation in plants and aid in the determination of the optimum screening methodology for selecting stress adapted genotypes. However, despite observations of TSM in many plant species, the study of this phenomenon in crop plants is in its infancy. Peanut is an ideal crop for addressing these questions because cultivated peanut species are self-pollinated (Norden et al., 1973), making the progeny of inbred lines a very close genetic match to the parent plants. Observed variation in progeny phenotypes under identical environmental conditions is likely caused by TSM and related mechanisms rather than genetic differences between progeny. Despite their lack of genetic diversity between generations, cultivated peanut species have high levels of ecophysiological plasticity (Awal and Ikeda, 2002), suggesting a role of TSM in determining peanut phenotypes. For these reasons, five distinct peanut genotypes were chosen to achieve the aim of quantifying the effects of TSM on the growth and vigor of seedlings, specifically regarding seedling establishment and root growth.

Section snippets

Seed source

Seed utilized in the current study was collected from a field experiment conducted at the Plant Science Research and Education Unit in Citra, FL, USA (29.4086, -82.171133), in which five peanut genotypes received either a water-deficit treatment or full irrigation (Zurweller, 2017). Two of the five genotypes examined, New Mexico (NM) Valencia C (Reg. No. 24, PI 565461) and COC 041 (PI 493631), were of the subspecies fastigiata (Arachis hypogaea L. subsp. fastigiata Waldron var. fastigiata

Seed and seedling characteristics

The results of the study indicated two primary patterns in the traits involved in seed weight and subsequent seedling vigor and establishment. There were strong differences among genotypes, as might be expected from the diversity of germplasm utilized in this study, and there was clear evidence of TSM moderated through the interaction of PSH with genotype. Genotypes varied greatly in seed and vigor characteristics, including seed weight (g), leachate conductivity (μS g−1), seed water potential

Discussion

The importance of environmentally induced parental effects (i.e. TSM) in determining the phenotypes of offspring has been recognized (Lacy, 1998), especially when seed dispersal mechanisms dictate a high likelihood of offspring experiencing the same environment as parent plants. In such cases, TSM represents an adaptive mechanism that could improve offspring fitness. This research illustrates the wide variability in the adaptive strategies moderated by how and when TSM is expressed in two

Acknowledgements

This material is based upon work that is supported by the National Institute of Food and Agriculture, U.S. Department of Agriculture, under HATCH project number FLA-AGR-005478. Further support was provided by the National Peanut Board, under the Southern Peanut Research Initiative project number PID489SIDFL117BID1550, and the University of Florida Plant Breeders Workgroup. The authors also thank Dr. Brendan Zurweller for his role in creating the seed source for this project.

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