High-Temperature Effect on Plant Development and Tuber Induction and Filling in Potato (Solanum tuberosum L.)

Abstract

Heat stress significantly impacts the physiology of potato plants (Solanum tuberosum L.). Regardless of the phenological stage at which thermal stress occurs, the most notable effect consistently emerges in tuber production. Heat stress can disrupt photosynthesis, transpiration, and overall plant metabolism. It is known that various genes encoding enzymes and glucose and sucrose transporters respond to temperature changes, influencing the partitioning of carbohydrates toward storage organs. This disturbance leads to disruptions in starch formation in tubers, affecting their development, and subsequently, the yield and quality of tubers. Understanding these interactions is crucial for developing heat-tolerant potato varieties in the face of climate change resulting from global warming.

1. Introduction

The Intergovernmental Panel on Climate Change predicts a gradual increase in global temperatures, which will alter the geographical distribution of climate zones. This change will impact the distribution and abundance of many plant species, modify crop phenology, and reduce agricultural yields [1]. It is estimated that climate change will result in a reduction in global potato production by 18–32% [2].

Potatoes, ranking fourth in global food crops after rice, wheat, and corn, are crucial for worldwide food production. This crop yields more energy per unit area than any other and boasts the second-highest protein content after soy, providing an excellent balance of essential amino acids, particularly lysine [3].

Optimal potato development occurs in temperatures between 15 and 20°C [4], with yields ranging from 12 to 60 tons of tubers per hectare. However, observations show a decline in yield when the ambient temperature exceeds 24°C. This reduction is attributed to a combination of independent morphological, physiological, and developmental issues.

The generation of potato plants from seeds is vital for plant breeding. Although there is growing interest in true potato seed (TPS) production in some tropical and subtropical regions [5], most countries cultivate potatoes from seed tubers.

Potato cultivation undergoes various stages characterized by physiological and morphological changes. The sprouting of seed tubers (Figure 1), considered the interruption of dormancy, occurs when seed tubers have initial sprouts with identifiable nodes, recognizable by visible scale leaves. The description and interruption of the dormancy state in potatoes have been extensively documented [6]. Seed tubers can be planted with or without sprouts or cut into two or three pieces, which are planted independently. The conditions of humidity, light, and temperature in which they are stored for sprouting are crucial, as these sprouts determine many of the plant’s developmental characteristics.

Figure 1.

Tuber anatomy. Sprout started and, in the future, a whole plant will grow.

The number of sprouts that a seed tuber produces depends on both genotype and its previous development. According to the concept of the “physiological age” of the tuber: a “young” tuber exhibits apical dominance and produces a single sprout, whereas a tuber with more time loses apical dominance and forms several sprouts [7].

Plant emergence is defined as the appearance of a sprout from the soil, and its development and growth are described based on the appearance of individual leaves up to the stem. It is preferred to define the stages of shoot growth and expansion based on the number of nodes, as they are easily identified as points of leaf insertion into the stem and can be counted along the shoot [6].

Shoot growth is determined by the number of nodes along the stem from the soil surface, as no morphological differences defining the moment of maturity of individual leaves are observed [8].

Flowering begins with the appearance of the floral bud and extends until the first flower is fully open, marking the end of vegetative development [9].

Tuberization is a stage that occurs shortly before flowering. In plants derived from seed tubers, the initiation of stolons generally occurs soon after plant emergence when it has a developed shoot. In most cultivars, stolons initiate in the axillary buds of the basal nodes of the stem and then elongate. The extension of stolons depends on genotype and environment. Stolons generated near the soil surface tend to be longer and initiate tubers later than stolons formed more deeply in the soil and closer to the original tuber. Moreover, the transition from stolon to tuber involves significant changes in both cell division and growth events, influenced by hormonal levels, with specific transcription factors and small RNAs playing crucial roles in tuberization. Stolon elongation ceases at the initiation of the tuber, and thickening occurs at its apical part, defined as the point at which the stolon thickens to double its initial diameter [10]. Tubercle growth is not considered a distinct developmental stage but is defined as when tubers on 80% of stolons are over 10 mm in diameter and progress.

Tuber maturation begins with the suberization of the periderm to form distinct skin, and development concludes when tubers detach from the stolons. For the optimal development of crops of this species, recommended temperatures are 13°C during the sprouting period, 12–14°C for shoot growth of foliar development, 18°C during the flowering process, and 16–20°C during tuber formation [11]. On the other hand, 20°C is recommended as an optimal temperature for photosynthesis in some European potato varieties [12]. From an ecological perspective, considering the potato’s center of origin, its cultivation thrives at relatively cool temperatures. In the Andean region, likely the native habitat of the potato, the average temperature of the warmest month is 16°C [13]. In the United States, the highest yields are obtained in regions with cooler summer temperatures, while in Scotland and northern Europe, they occur in July when the average temperature is around 15°C [14].

This chapter will explore the effect of temperatures exceeding 24°C on the metabolism and development at each phenological stage of this crop and the implications for tuber formation.

2. Sprouting of the seed tuber and sprout growth

The seed is a crucial factor in every agricultural production process, and for potatoes, the tuber plays a pivotal role in generating a new plant, earning it the label “seed tuber”. The health and physiological condition of these tubers significantly influence crop yield [15]. Seed tubers can be planted intact or divided; to a lesser extent, cuttings and microtubers obtained through in vitro culture are also utilized (Figure 2). In all these scenarios, the genetic makeup remains unchanged, as clonal reproduction is involved. The utilization of sexual seeds is primarily reserved for plant breeding purposes.

Figure 2.

Microtubers structure. Microtubers obtained by in vitro culture.

Seed tubers are temporarily stored at low temperatures and ambient humidity to suppress tuber metabolic activity and inhibit the development of microorganisms [16]. To break dormancy, the relative humidity of the environment is usually increased, as sprouts tend to emerge at low temperatures [17]. It is essential for seed tubers to reach their optimal sprouting state when planting for better yields. Sprout formation depends on the potato variety, determining the rest or dormancy period and physiological age, which, in turn, relies on storage conditions.

As a vegetative reproductive organ, part of its physiological development in the plant and post-harvest, the tuber goes through a state of rest or dormancy, a period of relative inactivity before sprout formation. The latency period is characteristic of each variety, and its duration is crucial for planting [18]. This period ends with the initiation of the first sprout’s growth. The dormancy period is generally considered from the end of harvest until the emergence of sprouts [19].

It has been observed that during the dormancy period of tuber storage, the physiological maturation process accelerates at high temperatures, consequently reducing the dormancy period. This phenomenon is not limited to high temperatures; low temperatures can also shorten this process. The end of dormancy is characterized by the initiation of vegetative bud growth, often with the apical bud emerging first in a state of dominance, followed by the formation of sprouts. However, apical growth is not desirable as it may result in a single-sprout plant. Therefore, it is common practice to remove the tip of the sprout, inducing a state of multiple-sprout growth, stored at low temperatures and diffuse light [20]. Nevertheless, seed tubers in multiple sprouting may age rapidly, developing etiolated and weak sprouts that form unproductive plants [21]. Physiologically young seed tubers, unlike old ones, realize their full potential yield, and potato cultivation extends over a longer period, resulting in higher overall yields [22].

Environmental conditions can influence the duration of the dormancy period in seed tubers during their development. The most crucial condition is high temperature during tuber development; alterations in moisture content or nutrient depletion in the soil can modify seed tuber development and physiology, affecting dormancy [17].

Drought, salinity, and above all, heat, are environmental factors that can severely impact the growth and yield of potato crops [23]. The development of seed tubers requires a temperature between 6°C and 18°C for optimal stem elongation [24].

3. Emergency and plant development

The vegetative part of the potato comprises a generally short and shallow root system, stems capable of growing submerged in the soil, known as stolons, where tubers develop, and stems emerging from the soil bearing compound leaves, representing the photosynthetic portion of the plant.

The development of the potato plant is complex, whether it originates from True Potato Seed (TPS) or a seed tuber. When TPS germinates to form a potato plant, the root system develops from the radicle, growing into an axonomorphic root and later creating a system of adventitious roots through branching [25]. From seed germination, a single stem develops after cotyledon emergence, which then branches at different heights from the axils of the leaves of the main stem, forming a sympodium. Additionally, it branches at basal nodes, forming a variable number of stolons where tubers develop. In this case, a single inflorescence develops at the apex of the main stem [26].

When the plant originates from a seed tuber, the vegetative part consists of a variable number of stems, depending on the number of sprouts in the original tuber. These stems can develop either above or below the ground. Leaves grow on the aerial stems, and an inflorescence can form at the apex of each. In the submerged stems or stolons, the tubers develop [27]. Sprouting must be complete and adequate to generate productive plants with optimal growth. Altered sprouting can result in a single shoot with apical dominance, leading to abnormal stem development.

One of the crucial phenomena for vegetative development and tuber production is photosynthesis. The most suitable temperature for photosynthesis in potato plants is between 16°C and 20°C [28]. The measurement of chlorophyll a fluorescence, as a parameter of photosynthetic efficiency, has allowed deductions that plants cultivated under a low-temperature regime (18/16°C, day/night) experience less stress during the initiation stage of stolon growth compared to higher temperatures [29].

The optimal temperature for canopy-level photosynthesis is determined to be around 24°C [30]. However, temperatures above 25°C promote the formation of taller plants with more lateral branches and smaller leaves [31]. Although this delays or even inhibits the formation of stolons and the induction and growth of the tuber [32]. On the other hand, the combination of high temperatures with long days inhibits tuber growth, resulting in a significant reduction in yield [33]. This negatively affects metabolic processes at different stages of plant development, stem growth, and morphology, particularly the tuberization process [30, 32].

High temperatures adversely affect photosynthesis, transpiration rate, photochemical efficiency, leaf structure, stem growth, tuber growth, and overall yield. These negative impacts are further exacerbated by concurrent water stress [34].

During plant development under thermal stress, leaves increase stomatal conductance to reduce leaf temperature. However, if water is scarce, leaves decrease stomatal conductance to prevent transpiration loss, leading to reduced evaporative cooling and increased tissue temperature [35].

Well-irrigated potato plants exposed to moderate heat (30/20°C Day/Night) exhibit a 3.5-fold increase in stomatal conductance compared to low temperatures, accompanied by an improved net carbon assimilation rate [34].

High temperatures affect tuber growth more drastically than shoot growth because more dry matter is allocated to shoots than roots, stolons, and tubers [33, 36].

4. Flowering

Among all developmental stages of potatoes, flowering is the least studied, particularly regarding the potential impact of temperature increases. However, a recent study by Zhu and colleagues [37] revealed that the heat shock transcription factor SpHsfA4c, isolated from wild potatoes (Solanum pinnatisectum Dun), is predominantly expressed in the leaves and flowers of these plants. The study observed that the expression of the SpHsfA4c gene was induced by thermal stress, and plants with this gene demonstrated increased heat resistance, suggesting its potential for developing heat-tolerant potato plants.

In several plant species, a “florigen” exists—a molecule that induces flowering. This protein was first described in Arabidopsis thaliana and named FT (FLOWERING LOCUS T), considered a universal florigen [38]. In potatoes, there are FT-like proteins, such as StSP3D, acting as a florigen, and another crucial one, StSP6A, described as a “tuberigen” [39, 40].

5. Tuberization

Optimal tuberization concerning weight, number, and tuber quality per plant is promoted by long nights (less than 12 hours of daylight), low temperatures, and a moderate nitrogen supply. Conversely, tuberization is diminished by short nights, high temperatures, and nitrogen-rich fertilization [41, 42].

While numerous studies have explored factors influencing tuberization, with a particular emphasis on photoperiod, only a few have delved into understanding how high temperatures impact this process [43]. Tuberization is affected when temperatures rise, with observations indicating that temperatures exceeding 25°C strongly alter assimilate distribution, causing a delay in tuber formation and reduced tuber growth [4]. These responses vary among different cultivars [44], but it has been confirmed in various potato cultivars that temperature affects tuberization. However, the exact regulatory mechanisms remain unclear [43]. Therefore, comprehending how temperature increases affect the genetic regulation of tuberization [45] is crucial.

The FT-like protein StSP6A (SELF-PRUNING 6A) is the “tuberigen”, crucial for tuber formation [39, 40]. StSP6A is expressed in the leaves and translocates to the tips of stolons when tuberization begins [40]. Despite reports indicating StSP6A’s involvement in photoperiod-induced tuberization, it has been observed that silencing this gene in short-day cultivars delays tuberization. Conversely, overexpression in long-day cultivars induces tuberization, even in those not dependent on photoperiod, emphasizing that its regulation is primarily attributed to temperature [39]. Its expression decreases as this abiotic factor increases [34, 46, 47].

The transcript of StSP6A is suppressed by heat [34, 46]. Studies subjecting potato plants to different temperatures (22°C, 30°C, and 35°C) have shown that heat impacts tuberization [43]. The number and size of tubers were measured at 5 and 9 weeks, revealing a delay in tuberization (Figure 1).

The expression of StSP6A in leaves gradually increases in plants at 22°C but diminishes in those subjected to high temperatures [43]. However, when measuring gene expression, it remains relatively consistent across different temperature treatments. This suggests that the expression of StSP6A alone is insufficient to explain the tuberization delay. Thus, tuberization may result from the transcriptional and post-transcriptional regulation of StSP6A. This was corroborated in experiments with transgenic potatoes overexpressing StSP6A, where, under high temperatures, the number of tubers per plant recovered, but the overall yield did not [43].

The regulation of StSP6A occurs through a microRNA called SUPPRESSING EXPRESSION OF SP6A (SES), which targets StSP6A and is induced by high temperatures [43, 46]. SES regulates StSP6A at high temperatures by degrading it (targeting it for degradation). Additionally, it is known that StSP6A’s expression occurs in leaves, but the protein moves to the stolon, indicating a potential post-translational regulation as well [48].

Other studies have proposed additional regulators of StSP6A, such as the homolog of TOC1 (TIMING OF CAB EXPRESSION 1) described in A. thaliana. TOC1 responds to temperature as a transcriptional regulator suppressing StSP6A expression [34, 47]. Silencing StTOC1 increases the expression of StSP6A and enhances tuberization, suggesting that StTOC1 likely directly binds to the promoter of StSP6A [47]. Other regulators affect StSP6A, including CYCLING DOF FACTOR (StCDF1), StSP5G (SELF-PRUNING 5G), StCOL1 (CONSTANS-LIKE 1), and GIGANTEA, whose expression increases in high temperatures. However, their role in tuberization has been primarily described in the induction of tuberization by photoperiod [34, 40, 48, 49, 50].

This intricate network of regulators underscores the complexity of the molecular mechanisms governing tuberization in response to temperature, providing valuable insights for future studies aiming to enhance potato crop resilience under changing climatic conditions.

In the transcriptomic analysis conducted by Park et al., [43], other potential genes involved in the thermo-regulation of tuberization are suggested. Genes such as StCEN1 (CENTRORADIALIS) and StGA2ox1-1 show decreased expression, while StCOL1 increases its expression with temperature, along with StERF5-3 (ETHYLENE RESPONSE FACTOR 5-3). This list includes genes related to plant hormones like gibberellins, which negatively affect tuberization [43], and ethylene, which also delays tuberization [51].

Another factor influencing tuberization is sugar transport. Mokrani and colleagues [52] reported a higher accumulation of glucose, sucrose, and starch in leaves at low temperatures. In contrast, plants grown at higher temperatures exhibited lower carbohydrate levels in leaves, leading to early tuberization, likely due to accelerated tuber initiation metabolism. The authors note that gene expression levels in leaves during temperature decrease favor the conversion of sucrose into starch during tuber maturation. In many cultivars, temperatures above 23°C resulted in increased photosynthesis, causing a noticeable shift in metabolites between leaves and tubers, generally resulting in decreased tuber yield [34].

The tuber-filling stage, dependent on carbohydrate metabolism, is highly sensitive to heat. The carbohydrate content in the stem (glucose, fructose, and sucrose) is altered under heat stress. High acid invertase activity has been observed in the stems of plants under heat stress, reducing assimilate partitioning to the tubers and increasing transport to the leaves [4, 36]. While this increase in invertase activity promotes stem growth, it reduces the assimilates that should contribute to tuber filling, leading to increased starch synthesis in the tuber. This phenomenon was observed by reducing the activity of enzymes involved in starch metabolism at soil temperatures of 30°C [52].

Tuberization induction begins with the thickening of stolon tips, as assimilate transport shifts from apoplastic to symplastic in the subapical region of the stolon. This is accompanied by an increase in sucrose concentration in the symplast, inducing the expression of sucrose synthase [53, 54]. This shift decreases soluble invertase activity in the stolon [54].

Among the enzymes involved in tuber growth through the assimilation of translocated photosynthates to the stolon tip is AGPase (Adenine Diphosphoglucose Pyrophosphorylase), which is activated at low temperatures [55].

During photosynthesis, a series of primary reactions occur, involving sunlight, water, chloroplasts, pigment molecules associated with proteins forming antenna complexes, and two reaction centers. Enzymes are also involved in the formation of ATP and NADPH2. Additionally, Ribulose 1,5-bisphosphate Carboxylase-Oxygenase can catalyze both carboxylation and oxygenation of Ribulose 1,5-bisphosphate in the Calvin-Benson cycle. Carboxylation of Ribulose 1,5-bisphosphate results in two molecules of 3-phosphoglycerate, characterizing the cycle as C3 type. Oxygenation produces one molecule of 3-phosphoglycerate and another of 2-phosphoglycerate, which participates in the photorespiration process [35].

The potato plant typically undergoes the C3 photosynthetic process. It has been confirmed that high temperatures lead to increased photorespiration [56], consequently causing a considerable loss of carbohydrates in the photosynthetic leaves or storage organs [57]. This energy expenditure also results in a reduction in sucrose export to the tuber [36].

5.1 Tuber initiation

For tuber development, it is not only necessary to have stolons but also to form a sufficient leaf area to sustain the carbon fixation rate. The growth of tubers relies primarily on net photosynthesis rather than on previously accumulated photosynthetic products in the foliage [57]. The initiation stage is crucial, marked by the increase and subsequent suppression of StSP6A expression, facilitating tuberization [43].

Temperature plays a pivotal role in both the initiation and growth of tubers. Cool nighttime temperatures, coupled with a short photoperiod, favor tuber initiation [58]. The inhibitory impact of high temperatures on tuber initiation involves a common hormonal control that disrupts the balance between endogenous gibberellins and inhibitors such as abscisic acid [59].

Elevated temperatures can lead to excessive elongation of the stolon and its branching, resulting in chain tuberization and stolon growth in a process known as heat sprouting [60].

High temperatures promote the partitioning of dry matter in the stems while reducing it in roots, stolons, and tubers, thereby decreasing the number of formed tubers. Consequently, the negative feedback effect of high temperature, after stolon development begins, includes a reduction in tuber initiation, diminishing the demand for photosynthate translocation to them and adversely affecting the photosynthetic system [60, 61].

5.2 Tuber growth

Sucrose serves as the primary sugar translocated in many plants, with its synthesis catalyzed by sucrose phosphate synthase and sucrose-6-phosphate. Degradation, on the other hand, is facilitated by sucrose synthase or invertase. The control of photosynthate partitioning between sucrose and starch in leaves lies with sucrose phosphate synthase, while sucrose synthase is considered the principal enzyme for sucrose cleavage in various tissues.

Growing tubers exhibit heightened sucrose synthase activity and ADP glucose pyrophosphorylase, both of which decrease as tubers develop. The conversion of sucrose to starch and subsequent starch deposition in tubers is regulated by starch synthase and ADP-glucose pyrophosphorylase [62].

Under heat stress, carbohydrate partitioning in potato plants shifts from shoots to tubers, resulting in an overall reduction in plant yield [36]. The impact of heat stress on enzymes that control sucrose metabolism in potatoes is not yet fully understood. Studies by [43] indicate that the photosynthetic performance of StSP6A-overexpressing potato plants remains unchanged, suggesting that photosynthetic capacity does not account for the lack of tuber growth. However, at later stages (9 weeks), sucrose, glucose, and fructose content increases in leaves at high temperatures, regardless of StSP6A overexpression, indicating a correlation with sugar transport rather than accumulation [43, 48].

Inhibiting sugar transport may occur at the level of transporters, exemplified by the interaction between StSWEET11 transporter and StSP6A. This interaction hinders tuber filling, promoting sucrose transport through the symplastic pathway. StSP6A RNAi plants exhibit a more abundant sugar flow in the stem, indicating increased flow. Understanding how sugar transport to the tuber occurs at high temperatures requires further investigation [43].

Activities of enzymes like starch synthase and ADP-glucose pyrophosphorylase decrease at temperatures above 25°C, resulting in less conversion of sucrose into starch in initiated tubers [62, 63].

Sucrose transport from leaves to photosynthate-demanding tissues is facilitated by sucrose transporters susceptible to high temperatures [64]. However, the regulation of sucrose transporter genes and their impact on sucrose transport and loading in tubers at high temperatures remain areas of limited understanding. Elevated temperatures lead to decreased total tuber yield, with low nighttime temperatures increasing the number of tubers per plant [65].

In some cultivars, larger tubers are obtained at higher temperatures when fewer tubers are formed per plant. While elevated daytime and nighttime temperatures reduce tuber yield, high nighttime temperatures seem to have a more detrimental effect. Potato plants grown at 31/29°C compared to 19/17°C Day/Night exhibit reduced sucrose synthase activity, ADP-glucose pyrophosphorylase, and tuber growth rate [52].

Krauss and Marschner [66] found decreased starch synthase activity, lower starch content, and slower tuber growth rates in three potato cultivars when exposed to 30°C compared to constant temperatures of 20°C.

5.3 Tuber maturation

During the tuber maturation stage, elevated temperatures (25/22°C Day/Night) enabled plants to produce increased amounts of glucose and fructose in photosynthate-demanding organs. Conversely, plants grown under low-temperature conditions exhibited high sucrose phosphate synthase activity. The temperature rise during tuber maturation also impacts the biosynthesis of steroidal glycoalkaloids (SGA), compounds that are toxic to human health and remain unaffected by cooking [67]. Therefore, the temperature increase not only influences potato crop productivity but also poses risks to human health [68].

6. Conclusions

Heat stress significantly disrupts tuber production in potato plants, marking the most affected stage among all phenological stages. Heat stress induces changes in crucial physiological processes, including photosynthesis, transpiration, and overall plant metabolism, directly affecting crop performance. Genes encoding enzymes and glucose and sucrose transporters respond to temperature fluctuations, influencing the allocation of carbohydrates to storage organs and causing disruptions in starch formation in tubers. Given the vulnerability of potato plants to thermal stress, unraveling these interactions becomes imperative for the development of heat-tolerant varieties, particularly in the context of climate change and global warming.