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

Racette, Kelly; Rowland, Diane; Tillman, Barry L.; Erickson, John E.; Muñoz, Patricio; Vermerris, Wilfred

doi:10.1016/j.envexpbot.2019.03.006

Cited by 22 publications

(29 citation statements)

References 49 publications

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“…Our results along with other studies (Verhoeven & van Gurp, 2012;González, 2016;Münzbergová et al 2019, Racette et al, 2019 point also on the genotype specificity of the stress memory. The length and number of nodes of the main stolon (parental ramet) were significantly or marginally significantly affected by the drought timing, genotype and 5-azaC application (Table 1; Fig.…”

Section: Discussionsupporting

confidence: 88%

“…Previous studies investigated the role duration or intensity of environmental stress on induction of transgenerational effects (e.g. Boyko, 2010;Verhoeven & van Gurp, 2012;Rahavi & Kovalchuk 2013a, b;González et al 2016;Racette et al, 2019) but did not consider the temporal dynamics of the stress memory. For instance, study by González et al (2017) showed that the drought in parental generation can trigger adaptive stress memory in T. repens , i.e.…”

Section: Discussionmentioning

confidence: 99%

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Remember or not? For how long can a clonal plant remember drought stress?

Quan¹,

Münzbergová²,

Latzel³

2021

Preprint

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Stress can be remembered by plants in a form of ‘stress memory’ that can alter future phenotypes of previously stressed plants and even phenotypes of their offspring. It was shown that DNA methylation is among the mechanisms mediating the memory. It is not known for how long the memory is kept by plants. If the memory is long lasting, it can become maladaptive in situations when parental-offspring environment differ. We investigated for how long can a parental plant “remember” that it experienced a stress and pass the memory to its clonal offspring. We grew parental plants of three genotypes of Trifolium repens for five months either in control conditions or in control conditions that were interrupted with drought pulses applied for two months in four different time-slots. We also treated half of the parental plants with 5-azacytidine (5-azaC) to test for the potential role of DNA methylation in the stress memory. Then, we transplanted parental cuttings (ramets) individually to control environment and allowed them to produce offspring ramets for two months. The drought stress experienced by parents affected phenotypes of offspring ramets. Such a memory resulted in enhanced number of offspring side branches originating from plants that experienced drought stress maximally 6 weeks before their transplantation to control environment. We did not find any transgenerational memory in offspring of plants that experienced drought stress later than 6 weeks before their transplantation. 5-azaC also reduced the effect of transgenerational memory on offspring ramets. We confirmed that drought stress can trigger transgenerational memory in T. repens that is very likely mediated by DNA methylation. Most importantly, the memory was time limited and was gradually erased. We conclude that the time limited memory on environmental stress can be adaptive as climate tends to be variable and parental-offspring environmental conditions often do not match.

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Section: Discussionsupporting

confidence: 88%

Section: Discussionmentioning

confidence: 99%

Remember or not? For how long can a clonal plant remember drought stress?

Quan¹,

Münzbergová²,

Latzel³

2021

Preprint

View full text Add to dashboard Cite

show abstract

“…Stress memory is known to act during biotic or abiotic stress exposure in a maternal plant, such that physiological, genetic or morphological responses are affected in subsequent offspring (Herman & Sultan, 2011). This phenomenon known as TSM is known to exist in peanut, such that increased seedling vigour has been documented when the parental plant experienced drought stress (Racette et al, 2019). Surprisingly, the current study results indicated that the exposure to seed immaturity, perhaps a surrogate for a stress exposure, from prior generations potentially increased the tolerance of immaturity in the subsequent generations.…”

Section: Discussionmentioning

confidence: 99%

“…Primary root length and fine root length were calculated by summing the root length in different diameter categories as follows: PR = Σ of root segments with diameter ≤1 mm; and FR = Σ of root segments with diameter >1 mm. This root diameter cut-off was commonly used in peanut studies, with FR was considered to be primarily functioned as nutrient absorption and water uptake (Jin et al, 2008;McCormack et al, 2015;Racette et al, 2019).…”

Section: Laboratory Bioassays Of Secondgeneration and Third-generation Seedsmentioning

confidence: 99%

“…Furthermore, peanut is known to have the potential for physiological stress memory. Racette et al (2020Racette et al ( , 2019 reported that TSM existed in peanut and exerted influences on seed germination, seedling vigour, field emergence and yield of its offspring. Peanut has also been found to be particularly susceptible to immaturity, where immature seed has been shown to be less vigorous and to affect not only early development but also physiological function and production (Carter et al, 2019).…”

Section: Introductionmentioning

confidence: 99%

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Multiple‐generation seed maturity effects on seedling vigour in a production environment

Song

Tseng

Rowland

et al. 2021

J Agronomy Crop Science

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Maturity is not only critical for vigour and other seed quality characteristics but also impacts the subsequent plant performance. If these impacts on the subsequent plant are long lasting, the potential to produce vigorous, mature seed may also be affected.This scenario lends itself to the concept of seed maturity memory (SMM) -an understanding of how seed maturity may impact subsequent generations of plants and the vigour of the seeds with different maturity they produce. This study aimed to assess the existence and perpetuation of SMM in peanut, with an emphasis on early seedling vigour. Field physiological measurements and bioassay assessments were carried out on the second generation (G2) and third generation (G3) of peanut seeds with distinct parental maturity backgrounds. Our results suggested maintaining mature seed in both prior and offspring generations helped maintain high seed vigour in subsequent generations. The SMM effects varied between cultivars, with TUFRunner™ '727' exhibiting SMM, whereas FloRun™ '107' did not show SMM in the effects from first generation (G1) to G2 maturities. Overall, a seed resulting from parental plants established from immature seed somewhere in their pedigree was less vigorous than that maintained mature seeds in their pedigree. However, patterns of possible SMM were not always consistent, which could be partially attributed to differing environmental conditions each generation of seed experienced during development. These results highlight the importance of maintaining mature seeds in agricultural production and bring up the issue of ensuring seed maturity consistency during stress memory research assessing vigour characteristics.

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Time dynamics of stress legacy in clonal transgenerational effects: A case study on Trifolium repens

Quan

Münzbergová

Latzel

2022

Ecology and Evolution

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Stress can be remembered by plants in a form of stress legacy that can alter future phenotypes of previously stressed plants and even phenotypes of their offspring. DNA methylation belongs among the mechanisms mediating the stress legacy. It is however not known for how long the stress legacy is carried by plants. If the legacy is long‐lasting, it can become maladaptive in situations when parental–offspring environment do not match. We investigated for how long after the last exposure of a parental plant to drought can the phenotype of its clonal offspring be altered. We grew parental plants of three genotypes of Trifolium repens for five months either in control conditions or in control conditions that were interrupted with intense drought periods applied for two months in four different time slots. We also treated half of the parental plants with a demethylating agent (5‐azacytidine, 5‐azaC) to test for the potential role of DNA methylation in the stress memory. Then, we transplanted parental cuttings (ramets) individually to control environment and allowed them to produce offspring ramets for two months. The drought stress experienced by parents affected phenotypes of offspring ramets. The stress legacy resulted in enhanced number of offspring ramets originating from plants that experienced drought stress even 56 days before their transplantation to the control environment. 5‐azaC altered transgenerational effects on offspring ramets. We confirmed that drought stress can trigger transgenerational effects in T . repens that is very likely mediated by DNA methylation. Most importantly, the stress legacy in parental plants persisted for at least 8 weeks suggesting that the stress legacy can persist in a clonal plant Trifolium repens for relatively long period. We suggest that the stress legacy should be considered in future ecological studies on clonal plants.

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

Cited by 22 publications

References 49 publications

Remember or not? For how long can a clonal plant remember drought stress?

Remember or not? For how long can a clonal plant remember drought stress?

Multiple‐generation seed maturity effects on seedling vigour in a production environment

Time dynamics of stress legacy in clonal transgenerational effects: A case study on Trifolium repens

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