Potato, Solanum tuberosum, the most important non-grain food crop and essential crop globally, has been widely cultivated around the world for centuries. The significance of this plant is increasing due to high nutritional value of the tubers combined with the simplicity of its propagation. As a plant organ, tuber of potato, is mainly edible part of it and popular as nutrient for almost all nations. Tuberization in potato is a very complex biological occurrence affected by numerous ecological signals, genetics, plant nutrition and several different hormones. Many pests including nematodes limit potato tuber development that plant hormones play roles in nematode feeding cell formation. Parasitic nematodes, important pests which cause damage to plants, tubers, suck up nutrients from plants and weaken plant development and yield losses. Many genes involve in tuber development and plant response nematodes. The aim of this chapter is to demonstrate the new advances in the field of molecular host-nematode interactions and tuber development.
The production of potatoes has been expeditiously increasing in the last forty years, especially in industrialising countries. However, the average amount of potatoes produced in developing countries is only half that of developed countries. The reasons for this are that modern agriculture is quite different between both developed and developing countries, and only limited contributions have been observed on potato yields revealed by modern breeding strategies in developing countries . Because of these reasons, novel genes associated with yield, such as those related to flowering, tolerance to a/biotic stress conditions, and enhanced postharvest quality attributes should be characterised and introgressed into cultivated potato genotypes. The advances in different omic platforms (transcriptomic, metabolomic, and proteomic) not only reduces the costs but also provides expanded knowledge about diversity in crop genomes. The datasets provide an excellent resource for selecting new genetic resources (e.g., single nucleotide polymorphisms, SNPs arrays) for introducing agronomically important improved varieties. The better linkage maps, gene annotations and much easier deciphering the genes related to different quality parameters, such as tuberization have been provided by releasing of potato genome sequence . For example, 185 clones that had previously been SNP genotyped by the Solanaceae Coordinated Agricultural Project (SolCAP) and detected 981 features which represent a mixture of metabolites, and hydrolysed fragments of abundant proteins were examined . Therefore, with the help of new genetic technologies, the quicker screening of large populations which improve the identification of quality candidate traits and genes will be more accessible and chargeable .
Potato tuberisation (tuber formation) is a complex physiological phenomenon regulated by both exogenously (environmental factors) and endogenously (metabolic pathways, hormones and genes) [7, 8]. Contrary to most plants that develop from roots, potato tuber originates from an underground specialised stem or stolons, accumulates starch which results in enlargement in favourable conditions . This complex development process can be examined in four stages in its simplest form, which are stolon initiation, enlargement of apical and subapical parts of the stolon, cell divisions and enlargement for tuber is triggered, and resource storage (starch accumulation) until tuber reaches its final mass . The induction of tuberisation is favoured under conditions of long dark periods, cool temperatures, and low amount of nitrogen fertilisation, regulation of a graft-transmissible signal transported from leaves to stolon tips for tuber-inducing stimuli . Initiation of tuberisation signalling and the transition from stolon to tuber is a very dynamic process at the molecular level. Identification of FLOWERING LOCUS T (FT)-like protein (StSP6A), CONSTANS (CO), POTATO HOMEOBOX 1 (POTH1), StBEL5 transcription factor, and microRNA156 and-172 revealed the governing the tuber formation process in potato [12, 13, 14, 15]. In stolon tips, before the onset of tuber initiation, StBEL5/StKNOX complex coordinates hundreds of genes, including the genes involved in phytohormone synthesis . Signalling and crosstalk of phytohormones, abscisic acid (ABA), auxins, cytokinins (CKs), gibberellins (GAs), ethylene, and strigolactones (SLs), and other compounds, such as carbohydrates and organic acids are known to play important key roles in regulating the morphological events of tuber development .
Several biotic stress factors effect negatively on potato plants that plant parasitic nematodes which are among them cause significant damage to potato growth and tuber development.
2. Plant parasitic nematodes and host-plant interactions
Plant-parasitic nematodes are significant crop pests and cause billions of dollars around the globe . Plant-parasitic nematodes (PPNs) have more than 4,100 species in the world . They infect many crops encompassing from the Solanaceae family to Fabaceae and Poaceae families . Plant-parasitic nematodes may divide based on feeding behaviour as ectoparasites, semi-endoparasites, and endoparasites [19, 20]. Ectoparasites do not spend their life cycle within the plant. However, endoparasitic nematodes spend all their life cycle within plant hosts. Root-knot nematodes (RKNs) are best examples of endoparasitic nematodes that complete their life cycle within a plant after entering the root. The RKN (
During the pathogen attack, plants recognise pathogens with different pathogen recognition systems such as pathogen-associated recognition systems (PAMP) and damage-associated molecular patterns (DAMPs) [19, 24].
Many plant-parasitic nematode (PPNs) species cause damage in potatoes and decrease the tuber quality. There are many nematodes species are found in potato plants:
Among the plant-parasitic nematodes, RKNs are one of the most damaging nematode genera, particularly
Root-knot nematodes, which are found in the
Potatoes are exposed to diseases and pests while growing. Nematodes that damage the tuber due to the propagation of potatoes by tubers constitute a serious problem in potato production. Nematode species such as potato cyst nematodes, RKNs (
In the second stage, juveniles and males of
The second stage is the juvenile root-knot nematodes, an infective stage that is found in free form in the soil which enters the root tip . Chemotactic genes may be involved in host-finding strategies, e.g.,
In the second stage, juveniles move between the cells (without damaging cells) and reach the feeding site . Sugar transporter genes: Sugars Will Eventually be Exported Transporter (SWEET), vacuolar glucose transporter (VGT), tonoplast monosaccharide transporter (TMT), and sucrose transporter (SUT/SUC) genes may be involved during early infection of
During the feeding, the nematode creates a feeding tube where it inserts the stylet to release nematode secretions of glands to manipulate plant resistance and create a feeding site . Karyokinesis occurs without cytokinesis in nematode feeding sites termed giant cells in plant tissues . Several nuclei are found in giant cells, and giant cells are much larger than normal cells. The thickness of giant cell walls in the vascular cylinder is much higher than the thickness of neighbouring cell walls (CWs) induced by
3. Formation of galls and plant- nematode molecular interactions
Nematodes cause damage to plants by influencing the phytohormone structure and modify plant development to establish feeding sites in plants . Plant hormones such as auxin and cytokinin play an important role in forming a sedentary nematode (Cyst and RKN) feeding site . Auxin, a plant hormone, is involved in the formation of galls after infection of RKN,
Small RNAs are differentially expressed in the galls induced by
Pattern-triggered immunity (PTI) responses involve camalexin and glucosinolate biosynthesis that BAK1-dependent and -independent PTI are nematode recognition mechanisms in
Microbes attaching to endoparasitic phytonematodes: PTI-responsive defence genes, particularly jasmonic acid-mediated PTI marker genes TFT1 and GRAS4.1, are up-regulated following microbe infections and
Nematodes may modify several plant hormones for successful parasitism. Furthermore, each defined hormone co-ordinately stimulates (IAA, CKs, ABA, and JA) or suppresses (GAs) the formation of tuberization. Numerous researches have reported the importance of the hormones and the genes to play key roles in the synthesis for tuberization. In this part of the chapter, recent studies will be discussed by bringing together the genes related to hormones that are involved in the formation of potato tubers.
4. Hormonal regulation of tuberisation
With respect to the involvement of hormones, gibberellic acid (GA) has been described as one of the most important regulators for tuber development [72, 73]. It is the required hormone for the elongation of stolon meristems during the initiation of tuberisation . Copalyl pyrophosphate synthase (CPS), ent-kaurene synthase (KS), ent-kaurene oxidase (KO), GA-20 oxidase (GA20ox), and GA-2 oxidase (GA2ox) are described as the key enzymes involved in the synthesis of GAs. CPS is the first key enzyme of the gibberellin biosynthesis pathway, which can be stopped by mutating the CPS. However, there is no study that reveals the functioning mechanism of the
Auxin is an exceptional plant hormone. It plays pronounced roles in many plant developmental processes, including tuber initiation, which is crosstalk with gibberellin and strigolactone. In other words, at the initiation of tuber development, the number of GA decreases, whereas that of auxin increases in the stolon subapical region which results in a swollen stolon . The roles of auxin hormone in various biosynthesis metabolisms have been explained in detail . The amount of endogenous auxin positively correlated to tuber growth rate . If it is zoomed at molecular studies, changes in the expression of auxin transport (PIN gene family), auxin response factors (ARF), and Aux/IAA genes during the tuber initiation have been shown [85, 86]. Auxin transcription factor6 (ARF6) decreased its expression several-fold during the transition from longitudinal to transverse cell division at swelling stolon tips . In transgenic potato plants, tuber formation was stimulated by an additional auxin biosynthesis gene (
Abscisic acid (ABA) is also well characterised and has been shown to have a supportive effect on tuber development when applied exogenously and to act antagonistically towards GAs, auxins and cytokinins . However, the main role for ABA was determined as dormancy induction and maintenance by different working groups . Genes encoding most enzymes of the ABA synthesis pathway have been identified and cloned from different species . Over-expression of the ABA synthetic gene
Among the phytohormones, it has long been known that cytokinins (CKs) function as universal regulators of storage-organ formation in plants. It was previously shown that CKs have a stimulating effect on tuber formation [93, 94]. CKs are an agronomically and commercially important trait, as CK application before tuber formation can increase tuber yield . However, although there are many effects of CKs on tuber development, tuber development regulated by CKs has not been fully elucidated at molecular level. The role of CKs for tuberisation is closely related to differential expression level of the genes, which can directly reflect the changes of related protein levels and metabolism regulation. Over-expression of
Strigolactones (SLs), carotenoid-derived plant metabolites, have emerged as an important new plant hormone, making it more attractive than other endogenous plant hormones. They mainly regulate various aspects of plant architecture, including the inhibition of shoot branching . Because SLs is a new hormone class, knowledge about SLs related genes in tuberisation and their regulation is much less compared to other hormones. Transgenic potato plants generated by down-regulating
Potato tubers are generally consumed fresh, but they can also be consumed throughout the year. Therefore, it might be necessary to store them under favourable conditions for an extended period like from one growing season to another one. After the potato has completed its maturation process, they transit to the dormancy period, in which reserves of starch and protein are kept for future sprouts . A major commercial issue is dormancy breakage following sprouting, resulting in quality losses and reduced tuber marketability. CIPC ([isopropyl-N-(3-chlorophenyl) carbamate) is particularly important as a sprout suppressant for potatoes during storage. However, CIPC has been proven not to be safe for humans and the environment in recent years . Therefore, alternate sprout suppressant approaches, for example constant ethylene supplement, could be used to suppress post-harvest sprouting . Storing potato tubers which were treated with/without ethylene binding inhibitor 1-methylcyclopropene (1-MCP at 1 μL L − 1 for 24 h), in air or air enhanced with constant ethylene (10 μL L − 1) , revealed extended ecodormancy in the potato samples treated with grouping of ethylene plus 1-MCP, while the inhibited sprout elongation in exogenous ethylene treated samples. Moreover, at the molecular level, continuous ethylene application activated two genes coding 1-aminocyclopropane-1-carboxylate oxidase (ACO) and parenchymatic ABA catabolism via
The plant cell wall composed of mainly pectin, is a complex and dynamic network of polysaccharides. Cell wall compositions function in plant development, stress responses, shelf life and plant growth. Basically, the primary cell wall (CW) consists of cellulosic (1,4-β-D-glucan), hemicellulosic polysaccharides for example xyloglucan (XG), and pectic polysaccharides for example homogalacturonan (HG) and rhamnogalacturonans I-II, which are all explained very well in different studies . The recent vision of the plant cell wall (PCW) suggests that the relationship of cellulose–pectin is more extensive and makes more important contributions to wall biomechanical properties than was previously thought . The CWs of tuber tissues are constitute of cellulose and hemicellulose which hold together a large amount of pectic polysaccharides . The texture of plant products is highly affected by the cell wall structure, and modifications of this part of the cell are the biggest contributors to texture. Generally, during fruit maturation, enzyme activities of hemicelluloses (HCL), celluloses (Cel), β-galactosidases (β-Gal), polygalacturonase (PG) and increase to lessen the intercellular associations and accomplish cell seperation, ensuing in modifications in fruit roughness and softening [110, 111]. Potato tuber texture is one of the most important quality characteristics of cooked potato and an obviously dominant trait that influences consumer preference, as mainly affecting the taste, aroma, and mouthfeel of the storage roots in potato . Two types of potatoes that differ in terms of texture represented an extreme variant in textural properties. The expression levels of the genes encoding two important cell wall degrading enzymes, pectin acetylesterase and xyloglucan endotransglycosylase, were significantly higher in Phureja, an accession that greatly reduced cooking time compared to Tuberosum accession . In another recent study, the correlation between the texture of cooked potato and β-amylase activity shows the negative correlation between the enzyme activity and firmness in cooked sweet potato .
Moreover, various studies have been conducted to elucidate the cell wall mechanism and texture changes in potato tuber. For example, two potato varieties showing significant differences in texture (Yushu No 10 with soft texture, Mianfen No 1 with firm texture) have been recently characterised in terms of the cell wall composition content and cell wall-related enzyme activities . The ‘Yushu No 10′ have more than twice soluble pectin content than ‘Mianfen No 1′, but the unsolvable pectin ingredient was lower than that of ‘Mianfen No 1′. It has been an important correlation of gumminess and chewiness between hemicellulose activity of ‘Yushu No 10’, and ‘Mianfen No 1′ having an unimportant correlation with Cel, PG, HCL, and β-Gal enzymes .
Potato is a highly heterozygous crop. Therefore, genetic advance of this crop using conventional breeding is labour-intensive and time-consuming work. For this reason, genetic engineering offers an opportunity to progress a limited genetic gain whilst retaining the well-known advantages of traditional varieties. The genetically modified potatoes show developments in quality traits that benefit farmers , consumers , and for the land in terms of sustainability . In recent years, with the increasingly aggravated global warming conditions, the research concentrated more on generation potato crops tolerant against extreme conditions such as salinity and drought . However, due to the concept of this chapter, we try to cover the transgenic studies using cell wall related enzymes. Transgenic potato made by the introduction of the gene encoding rhamnogalacturonan lyase (RGL) from
High-throughput RNA sequencing (RNA-Seq) is a powerful tool for revelaing the variability of gene expression levels between different samples. An RNA-Seq was performed to investigate the potato tuber dormancy release process, and 5912 and 3885 DEGs (differentially expressed genes) from dormancy tuber (DT) vs. dormancy release tuber (DRT) and DRT vs. sprouting tuber (ST), respectively . In another study carried out by iTRAQ labelling strategy, a total of 1752 proteins associated with tuber dormancy release in DT, DRT, and ST were identified. lncRNAs generally have structural features of mRNA, with exceptional roles in DNA methylation, histone modification, chromatin remodelling, and other biological processes. Moreover, lncRNAs regulated the expression of target genes by interacting with DNA, RNA, and proteins . In a recent study, 235 potato miRNAs out of 386 lncRNAs differentially expressed during sprouting were identified as putative targets. The results provided lncRNAs were involved in the potato tuber sprouting process and identified their possible functions in dormancy and sprouting . Based on these results, it can be said that tuber dormancy release is a complex process, and the genes upregulated during this period suggest the activation of multiple mechanisms enabling the tuber dormancy release.
Enzymatic browning is a serious problem for both producers and the industry as the tubers can be affected during storage and distribution. This problem is usually overcomed by applying chemical and/or physical agents or storing the potato in controlled storage conditions . However, keeping harvested potato tubers at low temperatures causes physiological changes, such as photosynthetic capacity, electrolyte leakage, and respiration rates . Transcriptomic and proteomic analysis were carried out in potato tubers stored at 15°C, 4°C, and 0°C to examine the mechanism of cold responses during post-harvest storage. The results showed that sugar accumulation increased at low temperatures.
Moreover, fifteen heat shock proteins (Hsps) were upregulated by low temperatures, which may act to prevent damage from cold stress . Application of the CRISPR/Cas9 to induce mutations in the StPPO2 gene in the tetraploid variety ‘Desiree’ reduced up to 69% in tuber PPO (Polyphenol oxidase) activity and 73% in enzymatic browning in transgenic lines compared to control . This result demonstrated that the CRISPR/Cas9 system has been successfully used to generate new potato varieties that reduce enzymatic browning through specific regulation of a single member of the StPPO gene family.
Plant hormones are involved in the gall formation and tuber development of potato plants. Numerous nematode species infects potato and cause an adverse effect on plant development and crop quality. Specifically, CNs (
To improve future potato tuber quality, it should be worked with industry and academic groups to meet producer and consumer preferences. With molecular and improved phenotyping techniques, knowledge about the mechanisms affecting potato tuber development, texture and post-harvest storage conditions will be increased for potato tuber quality. Furthermore, this combined information will profit the improvement of new cultivars by enlarging sustainable agricultural practices and storing approaches. Therefore, the combination of novel molecular techniques (gene-editing technologies) and pre/post-harvest applications will help the improvement, protection and viability of upcoming tuber quality.
Conflict of interest
The authors declare no conflict of interest.