Abstract Maize rough dwarf disease is a common epidemic disease in large areas. Its epidemic and occurrence mechanism is a complex process. In this paper， the epidemiological characteristics and influencing factors of maize rough dwarf disease in Huang-Huai-Hai plain were elaborated based on the research results of maize rough dwarf disease at home and abroad for many years. The epidemic of maize rough dwarf disease is affected by many factors， such as the occurrence and virus carrying rate of the first generation small brown planthopper， accumulation of virus sources on gramineous crops and weed hosts， maize variety resistance， maize sowing date， maize growth period， crop layout， tillage system， climate and ecological environment. The key factors causing the outbreak and epidemic of maize rough dwarf disease are the planting of maize susceptible varieties， the meeting of maize seedling stage and the peak period of adult spread of the first generation of small brown planthopper.
　　Key words Maize rough dwarf disease; Rice blackstreaked dwarf virus; Small brown planthopper; Occurrence and epidemic
　　 Maize rough dwarf disease （MRDD） is a devastating viral disease that often occurs on maize crops. Once occurring， the disease is difficult to control， which presents a serious threat to corn production safety. The disease is highly prone to largescale epidemic in the North China Plain， especially in the Huang-Huai-Hai River Basin， including Jiangsu， Hebei， Shandong， Henan， Hebei， Tianjin， Beijing and other provinces and cities. Since the 1970s， there were totally 3 pandemics respectively occurred in the 1970s[1]， the mid1990s[2-3]， and at the beginning of the 21stcentury of 2005-2012. The last pandemic lasted for years， causing catastrophic losses to maize production. According to statistics， MRDD stricken area in Shandong Province was 164 700 hm2 in 2005， 198 000 hm2 in 2006， 226 700 hm2 in 2007， 800 000 hm2 in 2008， 533 300 hm2 in 2009. The rate of diseased plants was 20%-30% in seriously affected plots， 70%-80% in some plots， while in the severely affected plots， there was even total crop failure[4]， which forced to turn over land， seriously damaging farmers incomes. The epidemic and mechanism of the disease is an extremely complex process. However， since 2014， up to 2018， MRDD sporadically occurred in the Huang-Huai-Hai maize producing area. Therefore， the disease has been overlooked in recent years， and thus fewer research and reports have been done. But it may come back when the future conditions are appropriate， so it should not be taken lightly because of its intermittent epidemic. In order to better prevent problems before they occur， this paper further explored and analyzed the epidemic characteristics of MRDD in Huang-Huai-Hai maize producing area based on the research results and the research work in recent years in China， with the aim to provide scientific and technological support for the green control of the disease and the sustainable development of maize industry in China. 　　MRDD Pathogens and Symptoms
　　In the early stage of MRDD， there are transparent oilimmersed chlorotic dotted spots on the bases of cordate leaves and both sides of midribs. Then， the growth of the diseased plants is slow， the internodes are stout， the plants are short， the diseased plants are dwarfed， the back of leaves and sheaths have weathered white strips of varying thicknesses， the leaves are thick green， the top leaves are clustered， and the male and female ears are poorly developed. In severe cases， the plants are not able to sprout ears and bear fruits， resulting in reduced or even no yield of maize. The pathogens which can cause MRDD include Rice BlackStreaked Dwarf Virus （RBSDV）[5-6]， Maize Rough Dwarf Virus （MRDV）[7]， and Mal de Río Cuarto Virus （MRCV）[8-9]， all of which belong to the second group of Fijivirus， Reoviridae. On the other hand， RBSDV is the pathogen of MRDD in many places in China[6， 10-11]， while no situation has been found to the other 2 pathogens， but there was a report on the damage caused by Southern Rice BlackStreaked Dwarf Virus （SRBSDV）[12-14].
　　The pathogen of the virus disease can also do damage to rice and wheat， which can cause Rice BlackStreaked Dwarf Disease （RBSDD） and wheat green dwarf disease[15].
　　MRDD Occurrence and Epidemic Characteristics
　　MRDD is a pandemic disease[16]， characterized by fulminant， intermittent， and devastating， and the only virustransmitting mediator is the small brown planthopper. The fulminant epidemic of the disease is not only dependent on the cultivation of maize itself， but also on the occurrences and epidemics of RBSDV and wheat green dwarf disease of the preceding or next rice and wheat crops， which forms the annual infection circular chain of the diseases （Fig.1）. In the north of China， corn， wheat and rice are often planted in annual cycles in Jiangsu， Shandong， Henan， Hebei and other places located in the Yangtze River and Huai River region and Huang-Huai-Hai plain，   which can easily cause the rise and fall of the 3 diseases （namely， MRDD， RBSDV， wheat green dwarf disease）. Among the 3 diseases， the damage of MRDD is the most serious to maize， which determines the complexity of the mechanism of the occurrence and epidemic outbreak of MRDD. The epidemic of MRDD can be affected by the occurrence amount and virus carrying rate of the first generation of small brown planthopper adults in rice stubble wheat field， virus accumulation in gramineous crops and weed hosts， resistance of maize varieties， maize sowing period， maize growth period， crop layout， farming system， climate， ecological environment and a various of other factors. Among them， the key factors which can cause the outbreak of MRDD epidemic are planting maize varieties susceptible for diseases， and the coincidence of maize seedling stage with the peak spreading season of the first generation of small brown planthopper adults. 　　Relationship between disease resistance of maize varieties and disease prevalence
　　The disease resistance of maize varieties is closely related to the occurrence of MRDD， and it is one of the key factors affecting the epidemic. There is a big difference in resistance to MRDD amongmaize varieties， but there is currently no maize variety immuneto MRDD[16]. Sowing tests were carried out to 10 maize varieties during the most susceptible period of the disease （May 24） during the promotion and application in production in Pingyin of Jinanin 2009， and the results showed that Zhengdan 958， Yuqing No.1， Xundan 20 were susceptible with the disease index of 76.07， 89.64， 90.84， respectively， Jinan No.7， Tiantai No.16， Ludan 981 had mild incidence with the disease index of 20.51， 18.32， 42.86， respectively. Generally， the susceptible varieties have an early onset and long disease susceptibility period （sowing period from May 1st to June 10th）， serious affection， while the varieties with resistance to the disease have late onset， light damage， short disease susceptibility period （sowing period from May 20 to June 5）， and therefore the effect on maize growth and yield is small.
　　Relationship between the growth period of maize and disease epidemic
　　Maize can be infected with MRDD during the whole growth period， but the seedlings with younger ages are more susceptible to the disease， which can have greater effects on the growth and yield of maize plants. The 1-6 leaf stage of maize is generally the sensitive period of infection of MRDD， while the plants will have no yield if infected in the coleoptile stage to the 2 leaf 1 heart period. And after the 7-8 leaf period （over 10 visible leaves）， the resistance of the plants becomes stronger and stronger， making it relatively safer period. In this way， the onset leaf age of maize plant presents significantlynegative correlation with the severity of the disease[17-19]. The plants which affect the disease as early as the 4-5leafage tend to be the plants with the most serious affection （Grade 4）， plant height of less than 1/3 of the healthy plants， nearly no spike and tassel differentiation and no kernels. The plants affected the disease after 10 leaf age tend to have normal heading and fruiting， but the grain fullness is not as good as that of healthy plants. According to the artificial virus inoculating test， the disease index tends to be significantly higher when the inoculation was done in the coleoptile stage， 2 leaf 1 heart period than in any other leaf age stage from the coleoptile stage to the 2 leaf 1 hear stage[20]（Fig.2）. 　　Relationship between maize sowing date and disease occurrence and epidemic
　　Maize sowing period has a significant impact on the occurrence of MRDD[21]Appropriate maize sowing period can make the maize seedling stage avoid the peak spreading period of the first generation of small brown planthopper adults， thus reducing the disease. On the contrary， the inappropriate maize sowing period will lead to the coincidence of maize seedling stage with the  peak spreading period of the first generation of small brown planthopper adults， thus aggravating the disease. The sowing tests carried out in Jining， Taian， Zaozhuang， Jinan， Dezhou， Qingdao of Shandong over the years showed that sowing maize from May 10 to June 10 in normal years can easily result in the occurrence of MRDD， with the disease becoming worse. On the other hand， avoiding sowing during the period， such as the sowing of spring maize from late April to early May in Huang-Huai-Hai plain， the direct sowing of summer maize after June 10-15  intercropping in wheat field， can greatly relieve the disease. There are differences in the climatic and ecological conditions in different regions and years， so the peak spreading period of the virustransmitting media， the first generation of small brown planthopper adults is different， which can be more accurately predicted from the first generation of small brown planthopper in wheat field. In Shandong Province， the peak spreading period of the first generation of small brown planthopper in Ludong （eastern Shandong） and Lubei （northern Shandong） is generally later than that in Luxi （western Shandong） and Lunan （southern Shandong）.
　　Relationship between the growth and decline as well as virus carrying rate of small brown planthopper and disease epidemic
　　Relationship between the growth and decline of small brown planthopper and disease epidemic
　　The number of the media small brown planthopper is also an important factor affecting the severity of MRDD[22]. The number of small brown planthopper adultsgoing through the winter  determines the incidence of spring maize[34]， and the occurrence of MRDD in summer maize is only closely related to the growth and decline of the first generation of adultpests[18， 23-25]. In Shandong， the investigation results of 6 consecutive years （2007-2012） （Jining， Taian， Zaozhuang， Jinan， Pingdu.） showed that the first generation of small brown planthopper adults emerged and gradually migrated to maize from wheat since late May， and entered into the high emergence and migration period in early and midJune， forming the migration peak during the harvest of wheat， when the number of small brown planthopper in maize increased by 6-10 times than before wheat harvesting. The high migration period lasted about 20 d， and the migration peak about 5-7 d. The incubation period was about 20 d for the infected plants in the field， and after the incubation to around midJuly， the maize seedlings which had the emergence period encountered with the peak emergence and migration period of the first generation of adults showed the infected symptoms together quickly， appearing the occurrence peak of the diseases. In Shandong， the maize seedlings sown in May 15June 10 are in the 3-7 leaf age period， when the diseased plant rate is the highest. The 2nd5thgeneration of small brown planthopper mainly live on rice or weeds[1]， and will not play a role in the spread of MRDD. Sowing maize after June 10-15 after wheat harvest will not lead to the pandemic of MRDD any more. 　　a. The infected plants below 4 leaf age. Severity： grade 4， 1/3 or less of healthy plant height， whole plant infection， extremely dwarf， basically non-productive; b. The infected plants of 5-6 leaf age. Severity： grade 3， about 1/2 of healthy plant height， the whole plant infection， and the female ear of less than 1/2 of healthy ear; c. The infected plants of 7-9 leaf age.Severity： 2， about 2/3 of healthy plant height， whole plant infection， and the female ear of less than 3/4 of healthy ear; d. The infected plants of 10 leaf age.Severity： 1， about 4/5 of healthy plant height， short male ear axis， only upper leaves infection， with symptoms like waxy white protrusion; e. Healthy plants.
　　Relationship between virus carrying rate of small brown planthopper and disease epidemic
　　The virus carrying rate of overwinter generation of the wheat field and the first generation of small brown planthopper adults also significantly affect the incidence of MRDD[26， 34]. For 5 consecutive years from 2009 to 2013， the first generation of small brown planthopper adults were collected from the riceproducing areas of ricewheat continuous cropping area （Jining）， wheatmaize continuous cropping area （Jinan， Dezhou）， mountains （Taishan）， coastal areas （Rushan of Weihai）， as well as the wheat fields of Jiangsu， Anhui， Henan， Heibei， all of which lied in the Huang-Huai-Hai plain. The adults were collected from late May to early June every year， and at least 50 adultswere collected from each point. Then， RTPCR method and dotELISA method were used to detect the RBSDV carried rate. The results showed that the virus carrying rate showed a trend of decreasing year by year. For example， the average virus carrying rate was 36.6% with the highest of 43.8% in 2009， the average virus carrying rate was 32.6% with the highest of 43.2% in 2010， the average was 13.3% with the highest of 22.6% in 2011， the average virus carrying rate was 11.11% with the highest of 17.4% in 2012， the average of virus carrying rate was 9.01% with the highest of 12.5%. Therefore， the comprehensive analysis showed that the virus carrying rate decreased year by year. The investigation from 2009 to 2013 showed that the occurrence of MRDD also showed a downward trend， and MRDD had intermittent epidemic characteristics.
　　Accumulation of virus sources in gramineous crops and weed hosts
　　RBSDV， the pathogen of MRDD disease， hosts in a wide variety of plants， and the abundant virus sources of the disease is also an important cause of the epidemic of the disease. RBSDV can infect maize， rice， wheat， sorghum， millet and other crops and grass weeds， and accumulate viruses on it， which makes it convenient for the cycling transmission of the virustransmitting media small brown planthopper among these hosts. 　　The outbreak and epidemic of blackstreaked dwarf disease （RBSDD） on rice crops will also accumulate a rich source of virus for the outbreak of MRDD. Recent relevant research shows that in 2006-2014， RBSDD occurred in large area in the rice producing areas in Jiangsu， Zhejiang， Shandong， Henan， which were also the years when MRDD was prevalent in these corn producing areas[4， 27-28].
　　Relationship between temperature and disease epidemic
　　Temperature also has an important impact on the occurrence of MRDD. Warm winters and cool summers， less rain in springs， rainy summers， low temperatures are conductive to the development and reproduction of virustransmitting mediators， and thus MRDD are often serious[29]. The temperature in winter will affect the wintering of small brown planthopper， as well as the incidence of MRDD. The pests in all stages （eggs， nymphs and adults） can resist low temperature when going through the winter. The climate in Huang-Huai-Hai plain， like Shandong， Henan， Hebei， is warm temperate， and the local small brown planthopper can safely go through the winter in warm winter years. Hu et al.[30]found that the death rates of the nymphs and adults of small brown planthopper was 20%， 60% respectively after freezing for 3 h at -13.5 ℃.Therefore， the small brown planthopper can go through the winter safely in the years with the daily average temperature from -1 ℃ to 2-3 ℃ with the extremely lowest temperature over -13.5 ℃ from December to February in Huang-Huai-Hai plain， which leads to the safe wintering of the small brown planthopper nymphs， promoting the outbreak and epidemic of small brown planthopper and MRDD continued for 6-7 years since 2005.
　　Relationship between ricewheat continuous cropping wheat field and disease epidemic
　　In the wide wheatproducing areas of the Huang-Huai-Hai area such as Shandong， Henan and Hebei， most are wheat fields with corn and wheat rotation， and there are also areas where rice and wheat are rotated for a certain period of time， that is， ricewheat continuous cropping wheat field. Although the area is small， it plays an important role in the outbreak and epidemic of MRDD [31-32]. The reason is that the ricewheat continuous cropping wheat field provides a favorable biological chain for the annual reproduction of the transmitting media small brown planthopper. The investigations on the wintering small brown planthopper in Jining， Jinan of Shandong showed that the number of wintering small brown planthopper in ricewheat continuous cropping field is much higher than the number in maizewheat continuous cropping field. When the wheat is harvested， a great number of the first generation of small brown planthopper adults migrate to the maize in the ricewheat cropping field， resulting in the pandemic of MRDD. Years of investigation on MRDD showed that the occurrence and epidemic of MRDD were serious in the maize producing areas with ricewheat continuous cropping wheat fields， such as Jining， Linyi of Shandong， where rice were planted in large area， and the ricewheat continuous cropping area in Zaozhuang， Heze and the surrounding areas. On the other hand， for the maize producing areas which are far away from the ricewheat continuous cropping area， the occurrence was light in the areas like Taian， Dezhou of Luxi， Yantai and Qingdao of Shandong Peninsula. 　　In 2014， the maize variety Zhengdan 958 was planted for sowing test in the planting areas in Jining City with rice planting and Taian City planting area without rice planting. The results showed that the incidence of MRDD was significantly different. The investigation results on the high occurrence period of MRDD （July 23） showed that the disease affected rate of the maize planted since April 25 was 32.0% with the disease index of 12.86. Then， the disease became more and more serious with the delay of sowing period. The disease affected plant rate was over 98% for the plants sown from May 5 to June 5， and the disease index was over 58.29， resulting in serious yield reduction. Moreover， the disease index of the plants sown on May 15 and 20 was 100， almost had no yield， and the disease was lightened only in the plants sown on June 15. Moreover， the maize disease index was significantly smaller for the maize plants in Taian test area sown during the sowing period， and the period with serious occurrence was 20 d shorter than that in Jining city.
　　Effects of different planting patterns of wheat field after rice cropping on the occurrence of MRDD （small brown planthopper）
　　Small brown planthopper is an insect of the local wintering population， and wheat is the wintering host， while the rice stubble wheat field is the main wintering place for the wintering small brown planthopper. Therefore， the traditional farming habits in ricewheat continuous cropping areas provide good ecological chain environment for the small brown planthopper to go through the winters and summers， making it the major cause leading to the outbreak of small brown planthopper， thereby leading to the high incidence of MRDD in ricewheat continuous cropping areas. After the rice is harvested， ploughing the land before wheat planting can play a certain cleaning effect on the farmland， and has a significanteffect on the survival of the wintering small brown planthopper.The winter wheat field is relatively clean， and there is no residualrice stubble and dead leaves except the wheat seedlings， which can reduce the hidden place for small brown planthopper， deteriorate the biochain environment in which the small brown planthopper survive over the winter， and depress the base number of the wintering small brown planthopper in the spring wheat fields. On the contrary， sowing wheat before the harvest of rice can have the wheat seedlings grow together with the unharvested rice plants for a certain time no matter early or late， during which time small brown planthopper can migrate from the rice plants to wheat seedlings. It makes it easy for the small brown planthopper to find the surviving hosts and enough food， accelerating the reproduction of the population. Moreover， in winter， there are rice stubble and dead leaves in the wheat field， which provide good habitats for the wintering small brown planthopper， thereby increasing the base number of wintering small brown planthopper in rice stubble wheat field， which may aggravate extent of the disease in the coming maize field. 　　Conclusion
　　MRDD is an important maize virus disease caused by the transmission of small brown planthopper， which can be infested on maize， rice， wheat and many grass weeds. As the only virustransmitting mediator of the disease pathogen， small brown planthopper can spread in the local area in the Huang-Huai-Hai area， but also has the ability to migrate to long distance with the airflow. It plays a key role in the annual cycle infection circulation of diseases among different crops and weeds， and so the MRDD transmitted by small brown planthopper is a viral disease with a wide range of outbreaks. Any carelessness can result in serious economic losses. Amongthe many factors affecting the occurrence and epidemic of MRDD， the key ones for the occurrence of MRDD are planting disease susceptible maize varieties and the coincidence of maize seedlings with the peak spreading period of the first generation of small brown planthopper adults. Moreover， the growth period of maize （leaf age） also has a significant effect on the occurrence of MRDD. In maize production， the sowing period of maize has a great effect on the occurrence degree on MRDD， and the maize sowing period determines whether the maize seedlings can met with the peak migration period of the first generation of small brown planthopper adults， and the duration of the meeting， which can directly affect the severity of the disease[25]. Some experts believe that the large amount of virus sources in nature and the favorable meteorological factors are also important reasons for the occurrence of largescale MRDD[16， 33]. Different maize producing areas in the various provinces of Huang-Huai-Hai plain can sow the spring and summer maize in appropriate time according to the local agricultural progress of each place， which can significantly reduce the damage degree of MRDD.
　　Wheat， as the main wintering and breeding host of small brown planthopper in winter and spring， plays an important role in the propagation of MRDD. RBSDV infecting wheat can cause wheat green dwarf disease. In the field survey of rice stubble wheat field in Jining in 2012， the incidence of wheat green dwarf disease was about 18.6% on average， some reached more than 40%， but there was no affected plant in the wheat field with no rice stubble （maize， wheat stubble wheat field）. Since RBSDV cannot be transmitted by the eggs of small brown planthopper， the plants affected by wheat green dwarf disease were the major primary infection source of MRDD， and they were also an important bridge for the accumulation of RBSDV in wheat field in winter and spring and the mutual transmission between crops[1， 34]. From 2006 to 2013， there was one more important reason for the pandemic of MRDD in the maize producing areas in Shandong and even in the demonstration region within Huang-Huai-Hai plain， which was the planting mode of ricewheat continuous cropping. The common sowing of wheat before rice harvest provides good wintering place for small brown planthopper， which increase the base numbers and accumulate more virus sources on affected wheat plants. Moreover， the poor control of small brown planthopper in spring wheat field is also an important reason for the epidemic of MRDD. 　　There are many factors restricted the epidemic mechanism and occurrence degree of MRDD.  It is difficult to describe the whole extremely complicated process in brief， so further studies are required so as to provide more reasonable strategies for scientific and rational control of the disease.
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