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Professor Zeng Kaifang of Southwest University et al.: Research progress on the role of AP2/ERF transcription factors in regulating postharvest diseases of fruits and vegetables

 Last Update: 2022-11-14
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In the process of evolution, plants gradually formed a complex stress response signaling network in vivo in order to adapt to the environment, so as to improve the resistance of plants to various abiotic and biological stresses such as low temperature, high temperature, pest pests, and diseases
.
Fresh fruits and vegetables are common edible plants and an important part of residents' diet, but because they are rich in water and sugar, they are often affected by various physiological diseases and infectious diseases after harvest and during storage and transportation
.
In response to the stress of postharvest diseases, there is a complex regulatory network in fruits and vegetables to enhance the resistance of fruits and vegetables to postharvest diseases
.

Studies have shown that the AP2/ERF transcription factor superfamily plays an important role in the response of fruits and vegetables to various postharvest diseases, and this family of transcription factors can participate in the regulation of the growth and development of fruits and vegetables, and respond to
various biotic and abiotic stresses 。 In order to clarify the regulatory effect of AP2/ERF transcription factor on postharvest physiological and invasive diseases of fruits and vegetables, Li Ting and Zeng Kaifang* from the School of Food Science, Southwest University, summarized the distribution and quantity of AP2/ERF transcription factors in fruits and vegetables, and clarified their role and mechanism in responding to postharvest physiological and invasive diseases of fruits and vegetables, and introduced the research progress of AP2/ERF transcription factors in response to postharvest diseases in bananas, cucumbers, peppers and other fruits and vegetables.
In order to provide a reference
for the study of AP2/ERF transcription factors in other fruits and vegetables and the use of AP2/ERF transcription factors to enhance the resistance of harvested vegetables to diseases.

1.
Overview of AP2/ERF transcription factors

Structural characteristics and classification of AP2/ERF transcription factors

There are 1 or 2 unique AP2 DNA binding domains in the structure of AP2/ERF transcription factor, which contains 60~70 highly conserved amino acid residues, composed of 1 β-folded and parallel β-folded α-helix, which is defined as the AP2/ERF transcription factor superfamily
according to this structural characteristics 。 YRG (amino acid sequence) and RAYD (amino acid sequence) elements in the AP2 domain play an important role in DNA binding activity, and the YRG element located at the N-terminal of the domain is composed of about 20 hydrophilic amino acid residues, which can promote DNA binding through base and hydrophilic groups; The RAYD element at the C-terminal contains about 40 residues that can mediate protein-protein interactions through α-helices or by interacting with DNA grooves through the hydrophobic surface of α-helices
.

Distribution and number of AP2/ERF transcription factors in fruits and vegetables

AP2/ERF transcription factor was originally isolated from the model plant Arabidopsis, with the in-depth study of AP2/ERF transcription factor, in addition to tobacco, Arabidopsis and other model plants, the genome-wide identification
of AP2/ERF transcription factor family in pears, dates, kiwifruit, radish, celery and other fruits and vegetables has been basically completed.
For example, there are a total of 125 AP2/ERF transcription factors in Longan, of which 101 belong to the ERF/DREB subfamily, 19 belong to the AP2 subfamily, 4 belong to the RAV subfamily, and 1 belongs to the Soloist subfamily
.
Karanja et al.
found a total of 247 AP2/ERF transcription factors in radish, of which 113 belonged to the ERF subfamily, 99 belonged to the DREB subfamily, 25 were AP2 subfamily, 9 were RAV subfamily, and 1 was Soloist subfamily, as shown
in Table 1.

2.
Regulation of AP2/ERF transcription factor on postharvest physiological diseases of fruits and vegetables

AP2/ERF transcription factors regulate the response of fruits and vegetables to low temperature damage

After harvesting, fruits and vegetables are often kept fresh at low temperatures to extend the storage period, but the optimal storage temperature of different varieties of fruits and vegetables is different
.
Under low temperature conditions, the normal physiological activities and tissue structure of fruit and vegetable products originating in the tropics and subtropics are easily affected and cold damage occurs.
When the fruit and vegetable tissue is in an environment below the freezing point, the cells will freeze and break, and the surface of fruits and vegetables will change color and necrosis and frost damage
.
At present, the regulatory effect of AP2/ERF transcription factor in postharvest cold damage stress of fruits and vegetables has been studied, but the regulation of postharvest freezing damage in fruits and vegetables is not clear
.
When the temperature is lower than 13 °C, the banana fruit will be cold damage, the transcription factor MaERF10 in banana can respond to low temperature stress and methyl jasmonate (MeJA) treatment, MaERF10 and MaJAZ3 can synergistically inhibit the expression of JA biosynthesis-related genes through protein interaction, and play a negative regulatory role
in MeJA-induced banana fruit response to low temperature stress 。 MdERF72 is an ET positive regulation transcription factor in apples, and the calluses of apples overexpressing MdERF72 were treated at low temperatures, and it was found that the growth potential of transgenic apple calluses was significantly better than that of wild type, and MdERF72 could significantly enhance the cold resistance of apples
。 Storage at 0 °C can significantly induce upregulation of the expression of EjERF27, EjERF30, EjERF36 and EjERF39, and its transcription level is positively correlated with pulp lignification, in which EjERF39 can bind and activate the DRE element of the lignin biosynthesis gene Ej4CL1 promoter region, and can also form protein complexes with EjMYB8 and play a synergistic effect on the activation of Ej4CL1 , promote the lignification of loquat fruits at low temperatures, thereby aggravating the cold damage
of loquat fruits.

AP2/ERF transcription factors regulate the response of fruits and vegetables to heat injury

Hot water treatment is a common physical method for postharvest storage and preservation of fruits and vegetables, but if the temperature is not properly controlled, quality indicators such as hardness of fruits and vegetables will be seriously affected
at high temperatures.
High temperature treatment will promote the softening of kiwifruit fruits, thereby accelerating the deterioration
of fruit quality.
During high temperature treatment, the expression mode of AdERFs in kiwifruit fruit changed greatly, and the expression of AdERF7, AdERF9 and AdERF10 were all related to high temperature stress.
The study of 33 SmERFs transcription factors in eggplant found that most of the SmERFs were induced by stress, and the expression of SmERF16, SmERF18 and other genes continued to be upregulated under high temperature treatment, inducing eggplant to respond to
high temperature stress.

AP2/ERF transcription factor regulates the response of fruits and vegetables to enzymatic browning

Browning affects the appearance and nutritional value of fruits and vegetables during postharvest storage, reduces their antioxidant content, and reduces their nutritional value
.
Enzymatic browning is the main cause of
browning in fruits and vegetables.
In 'Royal Gala' apples, ERF106 was significantly upregulated under the activation of MYB10, and the biosynthesis of ET was regulated by activating the expression of key genes ACS and ACO related to ET biosynthesis, which improved the activity of polyphenol oxidase, thereby promoting the browning
of apple fruits 。 The expression of NnERF5 in lotus root was inhibited at low temperature, carbon dioxide modified atmosphere packaging and vacuum conditions, which was consistent with the browning process of lotus root, and there was a significant correlation between the expression of NnERF5 and NnPAL1, so it was speculated that the downregulation of NnERF5 could inhibit the expression of NnPAL1 gene and regulate the activity of phenylalanine ammonia lyase (PAL), thereby participating in the regulation
of browning of lotus root.

AP2/ERF transcription factors regulate the response of fruits and vegetables to high CO2 injury

High CO2 content in the storage environment of fruits and vegetables will cause high CO2 damage, causing brown spots and dehydration and wilting on the surface or pulp tissue of fruits and
vegetables.
Wu Wei et al.
found that DkERF8 and DkERF16 can play a transcriptional regulatory role in the promoter of the DkEGase1 gene downstream encoding hemicellulose degradation-related enzymes, and speculated that ERFs can respond to high CO2 treatment by participating in the degradation of cellulose and hemicellulose in the process of deastringency and softening of persimmon fruits.
When high CO2 is treated with kiwifruit, AdERF4 and AdERF6 are also induced to be expressed in response to stress
.

3.
Regulation of AP2/ERF transcription factor on postharvest infectious diseases of fruits and vegetables

Regulation of AP2/ERF transcription factors on postharvest fungal diseases of fruits and vegetables

Diseases caused by fungal infestation are one of the main causes of postharvest rot of fruits, for example, apple wheel streak disease caused by Botryosphaeria dothidea is an important disease
in apple production in China 。 Wang Jiahui et al.
found that the infestation B.
The expression of MdERF11 gene in apple fruits of dothidea increased significantly, and overexpression of MdERF11 could increase the SA content in apple calluses and induce the expression of EDS1, PAL, PR1, NPR1 and other genes in SA synthesis pathway and signaling pathway, thereby activating the defense response and enhancing disease resistance, while silencing MdERF11 would reduce its disease resistance
.
In addition, the transcription factor MdERF113 is also involved in the defense response to apple stria infection, and its regulatory effect may be similar to
that of MdERF11 。 VqERF112, VqERF114 and VqERF072 in wild Mao grape 'Danfeng-2' in China can actively respond to biological stress, and these three transcription factors can enhance the resistance of grapes to gray mold by inducing the expression of downstream disease-resistant genes AtNPR1, AtPR1, AtICS1 and disease resistance-related genes AtPDF1.
2, AtLOX3, AtPR3 and AtPR4 in response to JA/ET
。

Regulation of AP2/ERF transcription factor on postharvest bacterial diseases in fruits and vegetables

Most of the occurrence of bacterial diseases in fruits only exist before harvest, such as apple and pear fruit pear fire blight, citrus canker disease and yellow dragon disease, mango black spot, peach and plum fruit bacterial perforation disease, watermelon bacterial horn spot disease and bacterial fruit spot disease and other diseases, the current research on AP2/ERF transcription factor on the regulation of fruit bacterial diseases mainly focuses on fruit tree plant diseases, such as peach ERFs in the defense of fruit tree bacterial perforation disease plays a positive regulatory role, The overexpression of MdERF100 in apples in Arabidopsis has increased Arabidopsis resistance, while the regulation of bacterial diseases by AP2/ERF during postharvest storage of fruits has rarely been reported
。 In vegetables, eggplant wilt is a disease caused by Ralstonia solanacearum, and after R.
solanacearum infects eggplant, the expression level of 24 SmERFs changes, and a silencing system is constructed for 8 SmERFs significantly expressed, and it is found that SmERF66 and SmERF88 are involved in the regulation
of eggplant resistance to wilt.
Cassava is highly susceptible to bacterial blight due to pathogenic bacteria
.
When pathogenic bacteria are infected, multiple transcription factors such as MeERF08, MeERF33, and MeERF56 containing stress-responsive elements in the promoter region can respond, which can be induced to be expressed in strong pathogenic strains and inhibited in weak pathogenic strains, thereby playing a transcriptional regulatory role
in disease infection.

4.
Regulation mechanism of AP2/ERF transcription factor on postharvest diseases of fruits and vegetables

Participates in plant hormone signaling pathways and induces the expression of defense-related genes

AP2/ERF transcription factor is a key regulator of plant hormone signaling, which mainly relies on plant hormone signaling pathways such as SA, ET, JA to regulate
fruit and vegetable diseases.
SA is a common hormone that mediates plant defense, and the SA signaling pathway can activate acquired resistance (SAR) in plant systems, and with the accumulation of ROS, it participates in the regulation
of diseases by activating disease-related marker genes in the SA signaling pathway, including inducing the expression of a series of PRs genes such as PR1, PR2, etc.
In the ET-mediated stress response signaling pathway, AP2/ERF transcription factor, as an ET response factor, plays an important regulatory role
in the downstream.
1-aminocyclopropane-1-carboxylic acid synthase (ACS) regulates the biosynthesis of ET, and after ET is recognized by various ET receptors and binds to it, it inhibits the activity of CTR1 (constitutive triple response 1) kinase associated with the receptor, so that it cannot phosphorylate
the C-terminal of EIN2 (ethylene insensitive 2).
。 After EIN2 enters the nucleus, it can activate the transcription factor EIN3, and EIN3 can activate the transcriptional expression of downstream ERF1 and other transcription factors, which in turn plays a transcriptional regulatory role
in other ET response genes in the signaling pathway.
As a growth regulator in higher plants, JA participates in various physiological activities of plants, and its biosynthesis and signaling are closely related to
plant resistance.
JA/ET-mediated signaling pathways can trigger the induction of systemic resistance and activate disease-related genes
such as PR1b, PR3, and PR4.

Strengthens the defenses of the cell wall

In plants, the cell wall is a physical barrier against adversity stress and pathogenic bacterial infection, and is also an indispensable part of the signaling process, playing an important role in the defense response, and AP2/ERF transcription factor mainly mediates the lignin biosynthesis pathway to participate in the regulation
of cell wall defense ability 。 ERF139 in plants can participate in the lignin synthesis pathway by inducing the expression of genes related to secondary cell wall synthesis such as LAC5, LBD15, MYB86, etc.
, and the accumulation of lignin and the network structure formed between it and cellulose and hemicellulose enhance the physical barrier, thereby enhancing the resistance
of plants to stress 。 The expression of loquat transcriptional inhibitor EjAP2-1 was negatively correlated with fruit lignification, and the transcription factor interacted with EjMYB1 and EjMYB2 related to lignin biosynthesis, and had an inhibitory effect on the expression of Ej4CL1 promoter of lignin synthesis-related gene, and weakened the lignification phenomenon
of loquat fruit at low temperature by inhibiting lignin biosynthesis.

Participation in mitogen-activated protein kinase cascade signaling pathway by phosphorylation

Phosphorylation is also an important regulatory form for ERF transcription factors to respond to biological stress, and Pti4 encoded by defense-related genes can be specifically phosphorylated by PTO kinases, thereby enhancing the binding
of Pti4 to downstream target genes.
When pathogenic bacteria activate the mitogen-activated protein kinase (MAPK) cascade signaling pathway, it will trigger hormone signaling pathways such as SA and JA, mediate the expression of defense-related genes through the change of ERF transcription factor expression level, activate the activity of defense-related enzymes and induce the accumulation of antibacterial substances, and then regulate the physical barrier and biochemical defense response of fruits and vegetables in response to disease infection
.

Protein complexes are formed

AP2/ERF transcription factors also interact with other transcription factors to form protein complexes, which play a synergistic or antagonistic regulatory role
in downstream target genes.
As shown in Figure 1, DkERF8 and DkERF16 can form complexes by interacting with DkNAC9 protein during postharvest deastringency, which plays a synergistic role in the regulation of downstream gene DkEGase1 promoter, indicating that ERF can participate in the response
of persimmon fruits to high CO2 treatment through interaction with NAC transcription factors.

Conclusion

In general, AP2/ERF transcription factors play an important regulatory role in the process of fruits and vegetables responding to postharvest physiological diseases and infectious diseases, and the transcription factors of this family mainly rely on signal pathways such as plant hormones to induce or inhibit the expression of downstream defense-related genes, and accompanied by the activation of antioxidant defense system, the accumulation of PRs proteins, the enhancement of cell wall defense capacity and the change of disease resistance pathways such as phosphorylation, thereby regulating the low temperature damage, enzymatic browning, and other disease resistance pathways of fruits and vegetables.
Resistance to postharvest diseases such as fungal and bacterial infectious diseases
.
At present, there are many studies on AP2/ERF transcription factors in regulating disease resistance in rice, tobacco, Arabidopsis thaliana and other plants, and the research in fruits and vegetables focuses on growth, development, maturity and aging, and the role and mechanism of AP2/ERF transcription factors in regulating postharvest diseases of fruits and vegetables need to be further
explored.
It has been found that AP2/ERF transcription factors play a positive role in the regulation of postharvest diseases of fruits and vegetables, and the regulatory network involved in the transcription factors that aggravate postharvest diseases of fruits and vegetables needs to be further improved
.
In addition, with the development of molecular biology and high-throughput sequencing technologies, the selection of resistant varieties through genetic engineering has become an important means for the prevention and control of diseases in some crops, but there is a big gap
in the research of transcription factors that play an important role in regulating disease resistance 。 In the future, on the basis of existing research methods, molecular biology technology can be used to study AP2/ERF transcription factors in more other varieties of fruits and vegetables and their functions in the regulation of postharvest diseases, and further clarify the signaling pathways in which AP2/ERF transcription factors are involved in the regulation of postharvest diseases in fruits and vegetables, focusing on the similarities and differences of AP2/ERF transcription factors in the regulatory mechanisms of physiological diseases and infectious diseases, their role and mechanism in the regulatory process of combining multiple signaling pathways, and AP2/ The anti-disease signaling pathways and possible mechanisms
in which ERF transcription factors are jointly regulated by other family transcription factors.
Through gene overexpression and silencing techniques, the role
of AP2/ERF transcription factor in responding to postharvest diseases in fruits and vegetables can be considered from multiple perspectives.

About the corresponding author

Zeng Kaifang, professor and doctoral supervisor of School of Food Science, Southwest University, Chongqing talent.
Head of the Innovation and Entrepreneurship Demonstration Team "Chongqing Fruit and Vegetable Storage and Logistics Innovation and Entrepreneurship Demonstration Team"; Director of Food Storage and Logistics Research Center, Southwest University; Head of
the Chongqing Food Storage and Logistics Graduate Tutor Team.
Visiting scholar
at the Volcani Research Center in Israel, Cornell University in the United States, and the University of Leuven in Belgium.
Standing Director of Postharvest Science and Technology Branch of Chinese Horticultural Society, Standing Director of Packaging Dynamics Professional Committee of Chinese Society of Vibration Engineering, Member of Postpartum Pathology Professional Committee of Chinese Plant Pathology Society, Expert Member of Food Biotechnology Professional Committee of Chinese Bioengineering Society, Member of Agricultural Products Cold Chain Logistics Standardization Technical Committee of
the Ministry of Agriculture.
His main research direction is food storage engineering, and his research field is fresh agricultural product storage and logistics
.
He has published more than 200 related academic papers, obtained 15 authorized national invention patents, presided over 6 projects of the National Natural Science Foundation of China, 2 projects of the National Key R&D Program/National Science and Technology Support Program, and 3 sub-projects
.

About the first author

Li Ting, female, master student, graduated from School of Food Science, Southwest University, major: food science; Bachelor's degree in the College of Life Sciences, Sichuan Normal University, majoring in food quality and safety
.
At the undergraduate stage, he has won many university-level study scholarships, "three good students", "excellent student cadres", "excellent university graduates" and other honorary titles; The project won the first prize of the Sichuan Provincial College Students Biological and Environmental Science and Technology Innovation Competition
.
At the postgraduate level, he has won three first-class academic scholarships and the honorary title of "Advanced Individual in Graduate Campus Culture"; His research direction is postharvest biology of fruits and vegetables, and he has participated in 1 general project of the National Natural Science Foundation of China, participated in 1 special key project of Chongqing technological innovation and application development, and published 1 academic paper
.

This paper, "Research Progress on the Role of AP2/ERF Transcription Factors in Regulating Postharvest Diseases in Fruits and Vegetables", is derived from Food Science, Vol.
43, No.
15, pp.
312-319, 2022, authors: Li Ting, Wang Wenjun, Chen Ou, Yao Shixiang, Zeng Kaifang
.
DOI: 10.
7506/spkx1002-6630-20210727-324
。 Click to view information about
the article.

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