宋田麗, 周建建, 徐晨曦, 蔡曉鋒, 戴紹軍, 王全華, 王小麗

(上海師范大學(xué) 生命與環(huán)境科學(xué)學(xué)院 植物種質(zhì)資源開發(fā)協(xié)同創(chuàng)新中心,上海 200234)

植物硝酸鹽轉(zhuǎn)運蛋白功能及表達調(diào)控研究進展

宋田麗, 周建建, 徐晨曦, 蔡曉鋒, 戴紹軍, 王全華, 王小麗*

(上海師范大學(xué) 生命與環(huán)境科學(xué)學(xué)院 植物種質(zhì)資源開發(fā)協(xié)同創(chuàng)新中心,上海 200234)

植物硝酸鹽轉(zhuǎn)運蛋白不僅能夠吸收、運轉(zhuǎn)硝態(tài)氮,而且在植物其他生理過程中也發(fā)揮重要作用.重點介紹了硝酸鹽轉(zhuǎn)運蛋白在氮素吸收運轉(zhuǎn)、硝酸鹽積累、側(cè)根發(fā)育、激素運轉(zhuǎn)以及逆境響應(yīng)調(diào)控等方面的最新研究進展,并概括了硝酸鹽轉(zhuǎn)運蛋白的表達調(diào)控模式.

硝酸鹽轉(zhuǎn)運蛋白; 硝酸鹽積累; 根系發(fā)育; 激素轉(zhuǎn)運; 逆境響應(yīng)

0 引 言

硝態(tài)氮(NO3--N)是植物最重要的氮素營養(yǎng)之一,與植物的生長發(fā)育、形態(tài)建成、產(chǎn)量品質(zhì)密切相關(guān).因此研究硝態(tài)氮的吸收運轉(zhuǎn)對于增強作物的氮素吸收和轉(zhuǎn)運能力、提高氮素利用效率有重要指導(dǎo)意義.植物根系以主動運輸方式吸收土壤或環(huán)境介質(zhì)中的硝態(tài)氮,并運輸?shù)狡渌M織器官中.為適應(yīng)環(huán)境硝態(tài)氮供應(yīng)濃度的時空變化,植物進化出兩種硝態(tài)氮吸收系統(tǒng),低親和轉(zhuǎn)運系統(tǒng)(LATS)和高親和轉(zhuǎn)運系統(tǒng)(HATS),分別在外源NO3-物質(zhì)的量濃度為0.001～1 mmol·L-1和高于1 mmol·L-1時,由硝酸鹽轉(zhuǎn)運蛋白(NRT)的NRT1/ PTR和NRT2兩大轉(zhuǎn)運蛋白家族負責(zé)執(zhí)行[1].根據(jù)最新命名規(guī)則,NRT1/PTR家族用NPF(NRT1/PTR family)表示[2].在擬南芥中預(yù)測到53個NPF和7個NRT2成員,在其他植物中也陸續(xù)預(yù)測出大量的NRT家族成員(表1).隨著擬南芥NRT研究的深入,研究者發(fā)現(xiàn)NRT除具有硝態(tài)氮轉(zhuǎn)運功能外,還在植物信號感受、形態(tài)建成、發(fā)育調(diào)控及與環(huán)境相互作用等過程中發(fā)揮不可忽視的作用.因此,有必要對NRT最新研究進展進行綜述,以充分認識NRT的功能特征,解析復(fù)雜氮代謝相關(guān)生物現(xiàn)象,并為植物基因改良提供基礎(chǔ).

表1 不同物種NRT成員數(shù)目比較

注:表中數(shù)據(jù)來源于已發(fā)表文章、基因組數(shù)據(jù)庫及部分綜述[8]

1 蛋白結(jié)構(gòu)

不同物種NRT序列高度同源,具有相似的保守序列.擬南芥NPF屬于major facilitator super(MFS)家族的小肽轉(zhuǎn)運體(PTR)家族,一般含450～600個氨基酸,12個跨膜區(qū),在第6、7跨膜區(qū)之間,有一個大的親水環(huán)相連[3],在第5跨膜區(qū)有一個PTR家族的保守基序(F-Y-x-x-I-N-x--S-L)[9].NRT2屬于MFS家族的nitrate /nitrite porter(NNP)家族,其典型特征為具有12個跨膜結(jié)構(gòu)域,每6個跨膜區(qū)分成一組,中間由一個大的親水環(huán)連接[10],在第2和第3個跨膜螺旋結(jié)構(gòu)之間有一個廣泛的MFS序列(G-x-xx-D-x-x-G-x-R)[9,11],在第5個跨膜螺旋結(jié)構(gòu)上有一個NNP標志序列(G-W/L-G-N-M/A-G)[12].

2 生理功能

2.1氮素吸收運轉(zhuǎn)

擬南芥中幾個NRT成員功能較清楚.AtNPF6.3(AtNRT1.1)是一個雙親和性的誘導(dǎo)型硝酸鹽轉(zhuǎn)運蛋白,能感知外源NO3-的濃度而進行高低親和性的轉(zhuǎn)換,通過該蛋白質(zhì)序列N端的第101位的蘇氨酸磷酸化開關(guān)控制硝酸鹽吸收[13].AtNPF4.6(AtNRT1.2)在根的表皮細胞中呈組成型表達,AtNRT1.2突變擬南芥株系的LATS下降50%～70%[14].AtNRT1.3在擬南芥葉中的表達受NO3-誘導(dǎo),但在根中的表達受NO3-抑制[15].AtNPF6.2(AtNRT1.4)主要在葉柄細胞的液泡膜及葉脈表達,其功能是調(diào)控NO3-在葉片的分配,將NO3-儲存到液泡中,在調(diào)節(jié)葉柄和葉片的NO3-穩(wěn)態(tài)平衡中發(fā)揮重要作用[16].AtNPF7.3(AtNRT1.5)在擬南芥根中柱鞘細胞膜表達,其功能是將NO3-裝載到木質(zhì)部,在蒸騰拉力的作用下通過長距離運輸將NO3-運送到地上部分[17].相反,定位在木質(zhì)部薄壁細胞的AtNPF7.2(AtNRT1.8)和定位于韌皮部伴胞的AtNPF2.9(NRT1.9)的功能是將NO3-從木質(zhì)部卸載,三者共同參與調(diào)節(jié)NO3-在根系和地上部分的分配[18-20].AtNPF2.12(AtNRT1.6)僅表達于角果的維管束和胚珠的珠柄處,主要通過調(diào)控NO3-從母體向胚的運輸,進而影響胚的早期發(fā)育[21].AtNPF2.13(NRT1.7)主要在葉片韌皮部的薄壁細胞表達,其表達豐度受氮饑餓的誘導(dǎo)[22],負責(zé)將NO3-向韌皮部運輸,從而調(diào)控衰老葉片中NO3-的再利用[23].AtNRT2.1、AtNRT2.2和AtNRT2.4定位于根表皮細胞,需與AtNAR2.1結(jié)合才能激活高親和轉(zhuǎn)運活性[24].AtNRT2.1是誘導(dǎo)型HATS中的主要轉(zhuǎn)運蛋白,其突變體中的HATS活性下降了50%～72%.Atnrt2.2突變體HATS活性僅下降19%,說明Atnrt2.2是對AtNRT2.1高親和轉(zhuǎn)運活性功能的補充[25].AtNRT2.4和AtNRT2.5是定位于質(zhì)膜的高親和性轉(zhuǎn)運蛋白,主要在側(cè)根的表皮和葉韌皮部薄壁細胞表達,參與根系NO3-高親和性轉(zhuǎn)運和韌皮部NO3-的分配,并均受氮饑餓的強烈誘導(dǎo)[23,26];AtNRT2.5突變后,擬南芥高親和性NO3-吸收顯著受抑制,敲除AtNRT2.1、AtNRT2.2、AtNRT2.4和AtNRT2.5中任意3個基因均會顯著抑制植株的生長[26].

除擬南芥外,其他植物中部分NRT的NO3-轉(zhuǎn)運功能也得到驗證.水稻(Oryzasativa)OsNRT1.1a和OsNRT1.1b為低親和硝酸鹽轉(zhuǎn)運蛋白,主要在根中表達,缺氮下表達受抑制[27].OsNPF2.4為pH依賴的低親和硝酸鹽轉(zhuǎn)運蛋白,主要定位于表皮細胞、木質(zhì)部薄壁組織、韌皮部伴胞,能間接調(diào)控鉀在地上地下的再分配[28].OsNPF2.2為pH依賴的受NO3-誘導(dǎo)的低親和硝酸鹽轉(zhuǎn)運蛋白,主要表達于木質(zhì)部薄壁組織,其功能是將硝酸鹽從木質(zhì)部卸載,參與調(diào)節(jié)NO3-在根系和地上部分的分配,并在水稻的生長發(fā)育中起重要作用[29].OsNRT2.3a是高親和轉(zhuǎn)運蛋白,定位于質(zhì)膜,主要在木質(zhì)部薄壁組織中表達,受NO3-誘導(dǎo),在NO3-由根向地上部分轉(zhuǎn)運的長距離運輸中發(fā)揮重要作用[30].白菜(Brassicarapa)BraNRT2.1為誘導(dǎo)型高親和硝酸鹽轉(zhuǎn)運蛋白,主要表達于根細胞質(zhì)膜,能互補擬南芥atnrt2.1突變體的高親和硝酸鹽轉(zhuǎn)運功能[31].油菜(Brassicacampestris)BcNRT1在擬南芥的根尖和地上部分表達,原生質(zhì)體亞細胞定位于質(zhì)膜,根部表達受25 mmol·L-1NO3-誘導(dǎo),BcNRT1 mRNA注入爪蟾卵母細胞能誘導(dǎo)NO3-轉(zhuǎn)運,且BcNRT1能恢復(fù)擬南芥chl1-5突變體植株的硝酸鹽吸收功能,這些結(jié)果證明BcNRT1是一個低親和的硝酸鹽轉(zhuǎn)運蛋白[32].Gu等[33]對菊花(Chrysanthemum)CmNRT1和CmNRT2進行了功能驗證,發(fā)現(xiàn)CmNRT1能被10 mmol·L-1NO3-誘導(dǎo),轉(zhuǎn)化擬南芥發(fā)現(xiàn)其編碼一個組成型的低親和轉(zhuǎn)運蛋白;CmNRT2表達水平受NO3-誘導(dǎo),定位于質(zhì)膜,與CmNAR2有相互作用,共同負責(zé)NO3-的高親和吸收[34].通過爪蟾卵母細胞表達系統(tǒng)及膜片鉗技術(shù)發(fā)現(xiàn)葡萄(Vitisvinifera)VvNPF3.2是一個低親和轉(zhuǎn)運蛋白,能轉(zhuǎn)運NO3-和NO2-[35].蒺藜狀苜蓿(Medicagotruncatula)MtNPF6.8為誘導(dǎo)型低親和轉(zhuǎn)運蛋白,同時參與ABA由根向地上部分的轉(zhuǎn)載[36].

2.2硝酸鹽積累

硝酸鹽是一類極易在蔬菜特別是葉菜類蔬菜中高量累積的物質(zhì),過量攝入硝酸鹽對人體健康存在極大的潛在危害[37].研究發(fā)現(xiàn)一些NRT確實與植物硝酸鹽積累性狀密切相關(guān),可應(yīng)用于控制蔬菜硝酸鹽積累.擬南芥nrt1.4突變體植株葉柄中的硝酸鹽含量只有野生型擬南芥的50%～64%,而葉片中硝酸鹽含量則稍高于野生型葉片[16].鹽脅迫下擬南芥NPF2.3(一個參與根系溢泌的硝酸鹽轉(zhuǎn)運蛋白編碼基因,又稱NAXT1)缺失突變體中硝態(tài)氮由根系向地上部分轉(zhuǎn)運減少,地上部分硝酸鹽含量明顯下降[38].黃瓜(Cucumissativus)中發(fā)現(xiàn)與AtNRT1.7同源的CsNRT1.7基因,將其在擬南芥nrt1.7-2的T-DNA插入突變體中表達,發(fā)現(xiàn)葉片面積增加的同時硝酸鹽含量顯著降低[39].通過比較硝酸鹽積累差異的兩個大白菜品種的BnNRT1.1和BnNRT2.1基因表達量發(fā)現(xiàn),高(2 mmol·L-1)、低(0.2 mmol·L-1)硝酸鹽處理下,高硝酸鹽積累品種根、莖、葉中BnNRT2基因表達量均顯著高于低硝酸鹽品種,且其吸收速率也明顯高于低硝酸鹽品種,NRT1.1基因表達僅在根中有差異,推測NRT2可能是與品種間硝酸鹽積累差異相關(guān),而NRT1可能僅對根部硝酸鹽含量起部分作用[24].Quaggiotti等發(fā)現(xiàn)硝酸鹽積累差異的兩個玉米(Zeamays)雜交種,其根和葉中ZmNrt2.1基因時間表達趨勢與硝酸鹽積累量變化趨勢相符,可能與玉米硝酸鹽積累存在一定的相關(guān)性[40].對NRT功能的研究有助于從分子水平解釋蔬菜硝酸鹽積累機理,可為通過生物技術(shù)手段降低植物硝酸鹽積累提供理論和技術(shù)支撐.

2.3信號轉(zhuǎn)導(dǎo)

目前比較明確的參與NO3-信號途徑的NPF是AtNRT1.1,參與硝酸根信號途徑在基因表達、根系發(fā)育、種子休眠以及逆境響應(yīng)等過程的調(diào)控[41].例如,AtNRT1.1作為NO3-受體,通過CIPK23改變其第101位蘇氨酸位點(T101)的磷酸化狀態(tài)(低NO3-濃度下Thr101位點磷酸化,反之,去磷酸化),從而改變AtNRT1.1的低親/高親活性以及硝酸鹽初級響應(yīng).NRT1.1感應(yīng)的信號通過一些激酶(如CIPK8)和轉(zhuǎn)錄因子(NLP7、NLP6、SPL9和LBD37/38/39)傳遞給下游基因,影響下游基因(如NIR、NRT2.1和NRT2.2)的表達,調(diào)控硝態(tài)氮信號的初級響應(yīng)過程[42].NRT1.1傳遞的信號還可以磷酯酶C(PLC)、Ca2+作為第二信使,調(diào)控轉(zhuǎn)錄因子(TGA1/4)、硝酸鹽轉(zhuǎn)運蛋白基因(NRT2.1、NRT2.2和NRT3.1)及硝態(tài)氮同化(NIA1和NiR)等基因的表達;還可以在不依賴PLC、Ca2+的條件下,將信號傳遞給生長素受體AFB3,并進一步調(diào)控轉(zhuǎn)錄因子NAC4和OBP4的轉(zhuǎn)錄活性,調(diào)控根系形態(tài)建成[43].

2.4側(cè)根發(fā)育

硝態(tài)氮對根系發(fā)育起著重要的調(diào)控作用.低氮(0.5～10 mmol·L-1)促進擬南芥?zhèn)雀L,而高氮(>10 mmol·L-1)抑制側(cè)根生長;增加擬南芥根系局部區(qū)域的硝酸根濃度,可以顯著促進該區(qū)域側(cè)根的生長[30,44].根系局部供應(yīng)硝態(tài)氮條件下,低氮一側(cè)由于NO3-供應(yīng)不足以及NRT1.1將側(cè)根生長素(IAA)轉(zhuǎn)移,導(dǎo)致側(cè)根生長素濃度下降,進而抑制了側(cè)根發(fā)育;相反,高硝態(tài)氮濃度一側(cè)NRT1.1對生長素輸出功能受抑制,生長素大量積累,促進側(cè)根生長[45-46].在此過程中,NRT1.1還作為NO3-信號受體參與NO3-信號對根系形態(tài)的調(diào)節(jié),首先NRT1.1將感受到的局部高濃度硝酸根信號傳導(dǎo)給ANR1,促進ANR1的表達,然后調(diào)控未知的下游基因,促進側(cè)根的伸長[44,47].還有可能的途徑是生長素經(jīng)NRT1.1運輸后,其濃度變化信號傳遞給生長素受體AFB3,進而調(diào)控一些對生長素敏感的基因(如ARF、NAC4和OBP4)表達,導(dǎo)致植物主根伸長受抑制并誘導(dǎo)側(cè)根的生長[43,48].此外,NO3-被根系吸收還原后的含氮代謝產(chǎn)物,可以誘導(dǎo)miR393表達,而上調(diào)后的miR393抑制AFB3的表達[49],二者協(xié)同參與了植物根系發(fā)育的調(diào)控.除NRT1.1外,NRT2.1對根系形態(tài)建成也具有重要作用,NRT1.1傳遞的信號通過PLC、Ca2+傳遞給轉(zhuǎn)錄因子(TGA1/4),進而調(diào)控NRT2.1的表達[43].在極低NO3-濃度(0.01 mmol·L-1)條件下,NRT2.1抑制側(cè)根起始[50],而在0.5 mmol·L-1NO3-濃度條件下NRT2.1促進側(cè)根原基發(fā)育,并且通過調(diào)節(jié)NO3-的吸收量來決定側(cè)根發(fā)育狀況[51].

2.5激素轉(zhuǎn)運

硝酸鹽轉(zhuǎn)運蛋白還參與IAA、脫落酸(ABA)、赤霉素(GAs)、茉莉酸異亮氨酸(JA-Ile)等多種激素的轉(zhuǎn)運,并進而直接或間接參與這些激素參與的生理調(diào)控過程.NPF6.3(NRT1.1/CHL1)參與IAA的運輸,并受高硝態(tài)氮濃度的抑制,在局部供應(yīng)硝態(tài)氮根系的形態(tài)建成中起重要作用.根系局部供應(yīng)硝態(tài)氮條件下,由于NPF6.3(NRT1.1/CHL1)將更多IAA從側(cè)根運出,降低了側(cè)根中生長素濃度,從而抑制側(cè)根發(fā)育,相反,高硝態(tài)氮濃度一側(cè)生長素輸出受抑制,生長素大量積累,促進側(cè)根生長[45].NRT1.1的生長素轉(zhuǎn)運能力依賴于Thr101位點的磷酸化水平,在表達磷酸化形式NTT1.1-T101D的卵母細胞中生長素的轉(zhuǎn)運能力遠高于未磷酸化形式的NTT1.1-T101A[52].利用酵母雙雜交系統(tǒng)和LC-MS/MS激素含量檢測,Kanno等[53]發(fā)現(xiàn),擬南芥NPF4.6、NPF4.1、NPF4.2和NPF4.5可能參與酵母中ABA的轉(zhuǎn)運;NPF4.1除轉(zhuǎn)運ABA外,還參與轉(zhuǎn)運GAs和JA-Ile[54];NPF2.12(NRT1.6)和NPF5.6參與不同類型GAs的轉(zhuǎn)運[54].此外,Tal等[55]在擬南芥GAs轉(zhuǎn)運突變體中發(fā)現(xiàn),定位于根內(nèi)皮層細胞的NPF3過表達能極大促進GAs的跨膜運輸,且其表達受GAs抑制,說明擬南芥NPF3作為輸入載體可能也參與了GAs體內(nèi)的分配和活性調(diào)控.與擬南芥ABA轉(zhuǎn)運蛋白AtNPF4.6相似,Pellizzaro等[36]發(fā)現(xiàn),在爪蟾卵母細胞中注射蒺藜苜蓿MtNPF6.8(MtNRT1.3)和AtNPF4.6 cRNA,均能使爪蟾卵母細胞ABA吸收增加,說明MtNPF6.8也具有ABA轉(zhuǎn)運功能,同時還發(fā)現(xiàn)MtNPF6.8和ABA共同了參與NO3-抑制蒺藜苜蓿主根生長的調(diào)控作用.

2.6脅迫防御

NRT還在植物脅迫防御方面發(fā)揮重要作用,如在氣孔保衛(wèi)細胞中表達的AtNRT1.1,通過增加保衛(wèi)細胞中NO3-含量引起保衛(wèi)細胞去極化,促進氣孔張開,從而負調(diào)控植物的干旱耐受性[56].NRT1.8參與的硝酸鹽分配在耐鎘脅迫中起著重要的作用.鎘處理下AtNRT1.8顯著上調(diào)能使更多的NO3-從地上部分運輸?shù)礁?根部較高濃度的NO3-有助于根系適應(yīng)鎘脅迫.相反,atnrt1.8突變體的根中NO3-比例較低,其根的伸長和植株生長也受抑制[18].硝態(tài)氮供應(yīng)條件下,AtNRT1.5的功能下調(diào)或缺失能增強植株鹽脅迫、干旱脅迫以及鎘脅迫等許多脅迫的耐受能力.與野生型植株相比,鹽處理下atnrt1.5突變體木質(zhì)部汁液中的Na+含量顯著下降,植株地上部的Na+含量降低而根中的顯著增加,使得atnrt1.5突變體耐鹽能力顯著增強[20].滲透脅迫下,atnrt1.5突變體根和地上部分抗旱相關(guān)功能基因P5CS1和RD29A的表達豐度顯著高于野生型植株,且抗旱能力也明顯強于野生型植株[20];當(dāng)把硝態(tài)氮換成銨態(tài)氮,atnrt1.5突變體對于這些脅迫的耐受能力不復(fù)存在.研究表明,逆境條件下NRT1.5和NRT1.8對植物脅迫耐受能力的調(diào)控與其介導(dǎo)的NO3-由地上向根部大量積累有關(guān),ET/JA(乙烯/茉莉酸)-NRT介導(dǎo)的信號途徑通過促進NRT1.8表達而抑制NRT1.5表達參與了逆境下NO3-的向根分配[57].

2.7提高氮素利用效率及其他

轉(zhuǎn)基因試驗證明NRT與作物產(chǎn)量和氮素利用效率密切相關(guān).Fan等[58]發(fā)現(xiàn)不同硝態(tài)氮供應(yīng)水平下,OsPTR6過表達都能夠增加水稻生物量,并提高了水稻氮積累量和谷氨酰胺合成酶活性;OsNRT1.1a和OsNRT1.1b過表達水稻植株地上部分生物量明顯增加,且OsNRT1.1b過表達植株的總氮含量更高,在低氮條件(0.125 mmol·L-1NH4NO3)下仍明顯高于野生型,說明OsNRT1.1b較OsNRT1.1a更能夠促進低氮下水稻對氮的吸收,提高作物的產(chǎn)量和氮素利用效率[27,59].Fan等[60]還發(fā)現(xiàn)OsNRT2.3b高表達水稻有著更強的pH緩沖能力,可以增強氮素、鐵、磷吸收能力,OsNRT2.3b過表達水稻根和地上部分的總磷含量在300 μmol·L-1無機磷(Pi)處理下比野生型分別增加了102%和75%,10 μmol·L-1Pi條件下增加了63%和62%.因為氮和磷是水稻生長最重要的兩個大量元素,因此過表達OsNRT2.3b能夠顯著提高水稻籽粒產(chǎn)量和氮素利用效率,比野生型糧食產(chǎn)量和稻草產(chǎn)量分別增加了44%和25%[61].

此外,NRT在植物次生代謝產(chǎn)物運輸中也發(fā)揮重要作用.Payne等[62]發(fā)現(xiàn)長春花(Catharanthusroseus)CrNPF2.9基因經(jīng)病毒誘導(dǎo)的基因沉默(VIGS)后,異胡豆苷在液泡中大量積累,同時減少了下游生物堿的合成,且過表達CrNPF2.9導(dǎo)致異胡豆苷積累量提高10倍,說明定位于液泡膜的CrNPF2.9在異胡豆苷從液泡向細胞質(zhì)轉(zhuǎn)運的過程中發(fā)揮關(guān)鍵作用.

3 表達調(diào)控

NRT的表達及其功能的發(fā)揮受外界和內(nèi)部許多因素調(diào)控,如氮素濃度、pH、激素、非生物脅迫、光合產(chǎn)物[21,63]及翻譯后調(diào)控等[64](表2).

3.1氮素調(diào)控

氮素對NRT表達調(diào)控已有大量報道[65].根據(jù)NRT對NO3-供應(yīng)的響應(yīng)差異,通常將NRT分為誘導(dǎo)型和組成型.不同物種NRT對NO3-的響應(yīng)與擬南芥不完全一致,且表達部位也不盡相同,如AtNRT1.1受低濃度NO3-誘導(dǎo)表達,而低濃度NO3-對于黃瓜CsNRT1.1無顯著誘導(dǎo)效果,且高NO3-供應(yīng)時表達下調(diào)[6];AtNRT1.9主要在根部組成型表達,而CsNRT1.9在生長到第1、4、8周的黃瓜根中均未檢測到其表達,而在子葉和老葉中的表達極為豐富,且能被高NO3-或短時的NO3-供應(yīng)強烈地誘導(dǎo)[6].不同物種NRT同源序列對氮素調(diào)控響應(yīng)的差異,可能與其不同的生理功能有關(guān).此外,NO3-對NRT表達的調(diào)控具有明顯的時間動態(tài)變化特點.1 mmol·L-1NO3-處理3～6 h后,大麥根中HvNRT2.1、HvNRT2.2和HvNRT2.3轉(zhuǎn)錄水平達到最高,12～24 h后表達量已降低到無法檢測,而處理3～48 h內(nèi)HvNRT2.4的表達水平能一直保持較高水平[66].Sorgonà等[67]對玉米幼苗供給50 μmol·L-1NO3-,前4 h內(nèi)ZmNRT2.1的轉(zhuǎn)錄水平呈明顯增加趨勢,24 h后逐漸降低.

3.2激素調(diào)控

AtNRT1.1主要在根和莖的新生部位表達,其表達受到IAA的調(diào)節(jié).施加外源IAA對NO3-吸收速率以及AtNRT1.1基因表達量有明顯促進作用[68],對成熟根系施加IAA能促進側(cè)根發(fā)育[45].鎘與鈉脅迫產(chǎn)生的ET/JA信號通過EIL1調(diào)節(jié)了ERF的表達,并由此上調(diào)了NRT1.8的表達,而ET/JA信號通過EIN3/EIL1等下調(diào)了NRT1.5的表達,促進硝酸鹽向根部的轉(zhuǎn)運[57].

表2 部分植物硝酸鹽轉(zhuǎn)運蛋白的硝酸鹽及其他調(diào)控匯總

3.3環(huán)境脅迫調(diào)控及其他

環(huán)境脅迫能夠顯著影響植物NRT的表達水平.芥菜(Brassicajuncea)7個NPF編碼基因(BjNRT1.1,BjNRT1.2,BjNRT1.3,BjNRT1.4,BjNRT1.5,BjNRT1.7,BjNRT1.8)中,BjNRT1.1和BjNRT1.5在低溫、熱、鹽和滲透脅迫1 h時均上調(diào),可能與逆境適應(yīng)有關(guān),而BjNRT1.1和BjNRT2.1的表達水平在以上非生物脅迫處理24 h時均下調(diào),推測兩者可能在逆境導(dǎo)致的芥菜生長發(fā)育抑制中起關(guān)鍵作用[82].干旱土壤中小麥NRT編碼基因的表達,取決于小麥基因型、生長階段及氮素供應(yīng)狀況.不同小麥基因型的TaNRT1.1和TaNRT1.2表達不同,低親和轉(zhuǎn)運蛋白TaNRT1.1和TaNRT1.2的轉(zhuǎn)錄水平在XY6基因型中受干旱誘導(dǎo),卻在XY107基因型中受干旱抑制;高親和性NRT基因TaNRT2.1的表達在干旱脅迫時下調(diào),而TaNRT2.2和TaNRT2.3的表達與小麥生長階段和氮素供應(yīng)狀況有關(guān);小麥XY107基因型中TaNRT2.1的表達顯著高于XY6基因型[83].鎘脅迫下根部AtNRT1.1活性受抑制,但同時抑制了根對鎘的吸收[84].鉬是硝酸還原酶的金屬輔酶,是NR活性所依賴的元素,外施鉬元素草莓NRT1.1和NRT2.1表達水平上調(diào),NO3-向地上部分運輸及還原能力增強,氮素利用效率提高[85].此外,不同發(fā)育階段NRT表達不同,黃瓜CsNRT1.7是一種衰老誘導(dǎo)型基因,其在黃瓜老葉中的表達要明顯高于成年葉與幼葉,CsNRT1.7也能被低氮誘導(dǎo)表達[39].

4 總結(jié)與展望

隨著對NRT研究的深入,發(fā)現(xiàn)其不僅參與NO3-的吸收和轉(zhuǎn)運,還參與眾多的植物生理過程,在植物生長發(fā)育中發(fā)揮重要的作用.對NRT的功能研究正引起越來越多研究者的重視.然而到目前為止,對NRT的研究主要集中在模式植物如擬南芥和水稻上,在其他作物如葉菜中的研究還很少.葉菜是重要的經(jīng)濟作物,也是產(chǎn)量、品質(zhì)嚴重依賴硝態(tài)氮的作物,明確NRT在葉菜硝態(tài)氮吸收利用及生長發(fā)育過程中的作用可能對實現(xiàn)葉菜減肥增效的可持續(xù)生產(chǎn)具有重要指導(dǎo)意義.此外,雖然已從不同植物中克隆出了多個NRT編碼基因,并鑒定了一些NRT的功能,但由于NRT通常存在多層次調(diào)控模式及多個NRT之間的協(xié)同合作,并受外界環(huán)境變化和自身發(fā)育水平的調(diào)控,全面認識NRT的生理功能還比較困難.此外,NRT還參與硝酸根信號通路,能夠與信號途徑中激素、轉(zhuǎn)錄因子及一些下游基因發(fā)生相互作用,加上氮代謝與碳代謝的偶聯(lián)關(guān)系,使得NRT功能可能更為多樣,研究也更為復(fù)雜.傳統(tǒng)單一的生理學(xué)、分子生物學(xué)方法在NRT研究上存在明顯的局限性,綜合利用各種生理生化及組學(xué)方法,從系統(tǒng)生物學(xué)水平上解析硝酸鹽轉(zhuǎn)運蛋白的功能可能是以后研究的一個熱點和難點.

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(責(zé)任編輯:顧浩然,馮珍珍)

Progressinfunctionandregulationofnitratetransportersinplants

Song Tianli, Zhou Jianjian, Xu Chenxi, Cai Xiaofeng, Dai Shaojun, Wang Quanhua, Wang Xiaoli*

(Development Center of Plant Germplasm Resources,College of Life and Environmental Sciences,Shanghai Normal University,Shanghai 200234,China)

Nitrate transporters can not only uptake and transport nitrate in plants,but also play key roles in many other physiological processes.This article reviewed the multiple functions of nitrate transporter in nitrate accumulation,lateral root development,hormone transport,and stress tolerance,etc.The expression regulation of nitrate transporters was also discussed.

nitrate transporters; nitrate accumulation; root system development; hormone transport; stress response

Q 945.12; S 60

A

1000-5137(2017)05-0740-11

2017-08-31

國家自然科學(xué)基金青年基金(31601744);上海市自然科學(xué)基金(15ZR1431300)、上海植物種質(zhì)資源工程技術(shù)研究中心項目(17DZ2252700).

宋田麗(1993-),女,碩士研究生,主要從事植物分子育種方面的研究.E-mail:1903972321@qq.com

導(dǎo)師簡介: 王全華(1963-),女,博士,研究員,主要從事植物分子育種方面的研究.E-mail:wqh6352083@126.com

*

王小麗(1980-),女,博士,講師,主要從事植物營養(yǎng)生理與分子育種方面的研究.E-mail:wxl2006by@163.com