Transcription factors controlling biotic stress response in potato plants

Highlights

• Nine/67 TFs families related with biotic stress response in potato plants.

• Complex mechanism of transcriptional and post-transcriptional TFs regulation.

• TFs divergence in biotic stress response among related and distant species.

• Synteny will provide evolutionary information on the defensive role of TFs.

Abstract

Plants are constantly exposed to biotic stress factors that affect their growth, development, and productivity. This interaction involves complex molecular mechanisms of resistance, tolerance, susceptibility, and sensibility. Potato is an important crop around the world, not only as a commodity but also as crop model, so to understand its gene regulation is particularly useful. The role of Transcription Factors (TFs) in gene regulation in biotic stress response in potato was not summarized and analyzed in any previous review. In this article, an inventory of potato TFs involved in biotic defenses was retrieved. Nine (ARF, NAC, WRYK, AP2/ERF-ERF, AP2/ERF-DREB, ZFP, TCP, bZIP, and BELL) from 67 TFs families were identified as having a role in defensive responses in potato. Activation/inactivation of such TFs triggers diverse metabolic pathways allowing plants to produce defensive proteins, metabolites, plant hormones, and/or transcriptional and post transcriptional modifications. Also, in this review, the phylogeny of StARF6, StARF17, and StWRKY8 was studied. An alignment and its comparison between amino acid sequences with related and distant species were conducted. As conclusions, our findings suggest divergence by functional approaches since we found they were related to other biotic response genes as well with constitutive genes for growth and development, being necessary to investigate more about homology and orthology to define more accurately response patterns among multiple species. The regulatory mechanisms reported include regulation at the transcriptional level through growth regulators and post-transcriptional regulation through modifications that inactivate or activate the resulting protein. The overexpression and activity depend not only on the number of copies of a gene but also on the elements present in its structure and the interaction/dimerization with other proteins. Synteny studies might be further conducted in potato because most of the evidence is focused on homology between species or emphasis on other Solanaceae. Analyses of potato TFs will help to understand the evolutionary and domestication processes, as well as provide useful knowledge for potato breeding programs aiming biotic stress resistance to increase productivity.

Introduction

Plants are constantly exposed to stress conditions that affect their growth, development, and production. These conditions may be abiotic factors expressed as deficiencies or overabundance in the physical or chemical environment that include temperature, salinity, drought, flood, light, nutrients and phytotoxic compounds [1]. Also, plants are limited by biotic factors that are constantly challenging their integrity, such as viroids, viruses, bacteria, fungi, oomycetes, protists, mycoplasmas, nematodes, invertebrates and other plants. The interaction of plants with these biotic factors has been a focus of attention because of their phytosanitary impact for crop production. How plants defend themselves against diseases and pests is the basis to develop sustainable control methods [2].

Potato is an important crop for food security and consequently different studies have been conducted to study its reponse to extreme conditions. Potato has a very diverse distribution pattern, which provides traits diversity to assure quality, availability, and stability [3]. It is currently cultivated in 149 countries as a commercial relevant crop [4]. Research around the world focuses on the generation of new robust varieties resistant/tolerant against pests and diseases, and with the capacity to produce in extreme climatic conditions, at the same time with enhanced nutritional traits [5]. Up to date, 49 species of insects from different tropical, subtropical and temperate regions are reported as pests for potato, which affects yield causing global losses of almost 16% [4]. Moreover, the following fungal diseases affect potato production: early blight (Alternaria solani), wart (Synchytrium endobioticum), and late blight disease (the biggest crop threat) caused by the oomycete Phytophthora infestans [6]. Also plamodiophoraceae affect potato such as powdery scab (Spongospora subterranea). Different bacterial diseases have been reported affecting potato: the bacterial wilt (Ralstonia spp.), blackleg (Pectobacterium spp., and Dickeya spp.), common scab (Streptomyces spp.), zebra chip (Candidatus Liberibacter solanacearum), and the potato ring rot (Clavibacter spp.). On the other hand, at least 40 viruses and two viroids have been identified capable of naturally infecting potato and reducing for up to 50% of the crop yield. The management of vector populations and geographical crop distribution are critical in promoting a high-quality (disease and pests free) seed to ensure the crop sustainability [7]. In this way, it is critical to know about plant defense response mechanisms to cope with stressful biotic factors on the crop, and to develop genetic improvement programs.

Stress activates a wide range of plant responses such as changes in gene expression and cell metabolism which will affect the growth rate and crop yield [8]. Plant responses can be activated directly by a stress factor or indirectly such as loss of membrane integrity due to injury-induced stresses in multifactorial expression and it involves the plant developmental stage, tissue, genotype, specie and others features [1]. Molecular mechanisms explain very complexly how the plant overcome or tolerate stressful conditions, which include changes in the expression of genes as well in cell signal transduction where transcription factors and signaling molecules play important roles in cell homeostasis [1].

Transcription factors (TFs) are proteins that regulate gene expression through specific binding to cis-acting elements in the promoter regions of target genes. The fundamental control point and the ability to respond quickly to the environment for cellular activity is considered the stage of messenger RNA transcription (mRNA). RNA polymerase II (RNAPII) is the protein responsible for transcribing nuclear genes and for the pre-initiation complex (PIC) at core promoter elements (CPE), but its function is not possible without the interaction of multiple proteins including TF [9]. These TFs can act as activators or repressors and their effect is often conditioned on their interaction with other cofactor and corepressor molecules to modify the expression of the target promoters. Then, a functional PIC in the central promoter results from the combination of TF, chromatinated proteins and cofactors [9]. TFs that bind to CPE and participate in basal transcription are called general transcription factors (GTF) and are complexes of multiple subunit proteins that participate in the recognition of the central promoter, the fundamental nucleation of the transcriptional PIC RNAPII and the initiation of the transcript [10].

Plant genomes include more than 2000 genes that encode different TF families [9]. According to the information available in the specialized database on bioinformatics PlnTFDB [11] of the University of Postdam (http://plntfdb.bio.uni-potsdam.de/v3.0/), there are 63 families of transcription factors and 22 groups of other plant transcriptional regulators [11]. Based on the iTAK database of the Fei Bioinformatics Lab, Boyce Thompson Institute and USDA Robert W. Holley Center (http://itak.feilab.net/cgi-bin/itak/db_family.cgi?plant=4113), TFs families are classified in 67, from which 24 groups of transcriptional regulators are referred for potato [12]. The aim of this review was to summarize TFs involved with biotic stress responses in potato. At this moment, there is no other review that summarizes and analyses the role of transcription factors affecting biotic stress in this crop. Then, the information presented in this review can be useful as consulting material or starting point for preliminary assumptions involving TF and defensive plant response in potato. Besides, to study the degree of conservancy and similarity, phylogeny of selected TFs was constructed with potato related and distant species; moreover synteny examples cases were searched in the literature. Finally, conclusions were proposed as perspectives to better understand and manipulate plant defensive responses in potato.