Improving potato drought tolerance through the induction of long-term water stress memory

Highlights

• Tubers from plants growing under mild water stress (primed seeds) were collected.

• Plants from primed and non-primed seeds were submitted to a second water stress.

• Plants from primed seeds showed higher yield, antioxidant activity and Δ¹³C.

• Long-term water stress memory occurred mainly in improved potato varieties.

Abstract

Knowledge of drought tolerance in potato is limited and very little is known about stress memory in this crop. In the present study, long-term stress memory was tested on tuber yield and drought tolerance related traits in three potato varieties (Unica, Désirée and Sarnav) with contrasted yields under water restriction. Seed tubers produced by plants grown under non-restricted (non-primed tubers) and restricted (primed tubers) water conditions were sown and exposed to similar watering treatments. Tuber yield and leaf greenness of plants from primed and non-primed seeds as well as tuber carbon isotope discrimination (Δ¹³C) and antioxidant activity (AA) responses to watering treatments were compared. Higher tuber yield, both under non-restricted and restricted water regimes, was produced by primed Sarnav plants. The decrease of tuber yield and Δ¹³C with water restriction was lower in primed Unica plants. Long-term stress memory consequently appears to be highly genotype-dependent in potato. Its expression in plants originated from primed tubers and facing water restriction seems to be positively associated to the degree of inherent capability of the cultivar to yield under water restriction. However, other effects of priming appear to be genotype-independent as priming enhanced the tuber AA in response to water restriction in the three varieties.

Introduction

Potato (Solanum tuberosum L.), the fourth most important food crop worldwide [1], regularly experiences drought stress due to erratic rainfall or inadequate irrigation. Potato is considered to be rather susceptible to drought [2] and water shortage results in a reduction of tuber production [3] and quality [4]. Tuber yield is particularly affected by early drought stress [5], which hinders tuber initiation [6]. Given the recent expansion of potato cultivation to drought-prone areas [7] and the expected effects of climate change on rainfall [8], a better understanding of physiological mechanisms underlying drought tolerance is required. Traits that confer drought tolerance in potato include root depth [9], high root dry weight [10] particularly in the deep soil layers [11] and high capacity of osmotic adjustment [12]. Recent studies have shown that the temporal pattern of chlorophyll concentration is related to drought tolerance and is a useful trait to estimate it [13], [14]. Also, carbon isotope discrimination (Δ¹³C) in tubers has been reported to be associated to yield under drought stress in potato [15].

Although drought tolerance has been investigated in potato, very little is known about how potato germplasm responds to consecutive stresses. A previous exposure to different types of stress (or priming) can alter subsequent responses and eventually prepare the plant to more quickly or aggressively respond to future stress, referred to as stress memory [16], has been reported in diverse plant species [17], [18], [19]. Stress memory involves accumulation of signaling proteins or transcription factors and epigenetic mechanisms in plants (DNA methylation or acetylation, chromatin remodeling or histones alteration) that result in gene silencing and/or activation, leading to an improvement in the stress response when plants are exposed to a subsequent stress event [17], [20], [21]. Stress memory involves mitotic (short and long-term memory) and meiotic (transgenerational memory i.e. stress memory is transmitted to the non-stressed progeny, [22], [23]) inheritance. Short-term memory is confined to small time spans of less than 1 week [17], whereas long-term memory is defined as epigentic stress memory that could be maintained during subsequent development within the life span of an organism [21]. In sexually reproducing plants, vernalization and exposing seeds to some mild stresses (like saline solutions [24]) to condition a response or resistance in later phenological stages are examples of long-term stress memory. It has been suggested that in clonal plants like some perennial grasses, long-term memory could be carry over into sprouts harvested from primed individuals [25]. In potato, short-term water stress memory has been evidenced in some accessions of S. tuberosum spp. andigena after repeated drought stress. It is attributed to the transcription of genes related with the metabolic pathway of ABA, anthocyanin, antioxidants, heat-shock proteins and chromatin remodeling [26]. The higher drought stress tolerance of S. tuberosum spp. andigena, compared to S. tuberosum spp. tuberosum has been attributed to the induction of heat shock proteins and antioxidant genes encoding proteins in the chloroplast and genes for anthocyanin synthesis and transport that could be important in case of repeated stress [27]. It has not been yet determined, however, whether potato plants grown from tubers harvested from individuals having undergone water restriction in a previous growing season (or primed tubers) modified their response to water stress. The hypothesis of such long-term memory of drought stress has been tested in the present work in three potato varieties with contrasted tuber yield under water restriction. For this purpose, in this study tuber yield and several other traits related to drought tolerance (leaf greenness, tuber Δ¹³C, and antioxidant activity) were assessed in plants originated from primed and non-primed tubers. An effect of stress memory on antioxidant activity has been reported in Arabidopsis [28].