陸姣云,段兵紅,楊梅,楊晗,楊惠敏*
(1.草地農(nóng)業(yè)生態(tài)系統(tǒng)國(guó)家重點(diǎn)實(shí)驗(yàn)室,蘭州大學(xué)草地農(nóng)業(yè)科技學(xué)院,甘肅 蘭州 730020;2.中國(guó)科學(xué)院遺傳與發(fā)育生物學(xué)研究所,植物基因組學(xué)國(guó)家重點(diǎn)實(shí)驗(yàn)室與植物基因研究中心,北京 100101)
20世紀(jì)20年代,植物學(xué)界就已經(jīng)認(rèn)識(shí)到植物養(yǎng)分利用效率在植物研究中的重要意義。1986年,Killingbeck[1]首次明確提出養(yǎng)分重吸收(nutrient resorption)的概念,從另一個(gè)角度對(duì)植物養(yǎng)分利用進(jìn)行了闡釋。植物將衰老組織中的部分養(yǎng)分轉(zhuǎn)移到其他組織的過(guò)程稱為養(yǎng)分重吸收[1]。生長(zhǎng)在貧瘠環(huán)境下的植物養(yǎng)分保存效率較高,可能并不是因?yàn)樗鼈儗?duì)土壤養(yǎng)分的吸收能力更強(qiáng),而是因?yàn)轲B(yǎng)分重吸收更充分[2]。對(duì)植物而言,重吸收可以提高養(yǎng)分(主要如氮N和磷P)利用效率,降低植物生長(zhǎng)對(duì)土壤養(yǎng)分條件的依賴程度[3-9]。重吸收能延長(zhǎng)養(yǎng)分在植物體內(nèi)的存留時(shí)間,為生長(zhǎng)組織所需的生物量生產(chǎn)充實(shí)了物質(zhì)基礎(chǔ)[10]。此外,養(yǎng)分重吸收還有助于減少因凋落物分解、淋溶造成的養(yǎng)分損失[11]。因此,養(yǎng)分重吸收增強(qiáng)了植物對(duì)養(yǎng)分貧瘠環(huán)境或因逆境(如干旱)導(dǎo)致的養(yǎng)分獲取困難環(huán)境的適應(yīng)能力[3,12-15],體現(xiàn)了植物對(duì)環(huán)境多樣性的適應(yīng),是植物增強(qiáng)競(jìng)爭(zhēng)力、提高生產(chǎn)力和適應(yīng)逆境的重要機(jī)制之一。
養(yǎng)分重吸收易受多種因素影響,不同植物的養(yǎng)分重吸收不同,同一種植物對(duì)不同時(shí)、空環(huán)境變化的響應(yīng)也有差異。因此,深入研究養(yǎng)分重吸收變化規(guī)律,闡明調(diào)控機(jī)制,有助于充分了解系統(tǒng)養(yǎng)分運(yùn)動(dòng)規(guī)律和調(diào)控機(jī)制,并可根據(jù)養(yǎng)分重吸收強(qiáng)度(重吸收效率和重吸收度)評(píng)估整個(gè)系統(tǒng)的生產(chǎn)力水平、土壤養(yǎng)分循環(huán)速度等,從而為系統(tǒng)的科學(xué)管理提供參考。本文綜述了環(huán)境因子和遺傳特性對(duì)植物葉片氮磷養(yǎng)分重吸收的影響,重點(diǎn)闡述了重吸收在不同因子影響下的響應(yīng)規(guī)律,并分析其調(diào)控機(jī)理。
植物養(yǎng)分重吸收強(qiáng)度多以養(yǎng)分重吸收效率(nutrient resorption efficiency,NuRE,從衰老組織轉(zhuǎn)移到幼嫩組織中的養(yǎng)分比例)[6]來(lái)表征。高養(yǎng)分重吸收效率使植物更少地依賴于當(dāng)前的養(yǎng)分吸收并增加了植物(尤其是養(yǎng)分貧瘠的生態(tài)系統(tǒng))的適應(yīng)性[16]。養(yǎng)分重吸收效率可以通過(guò)下式計(jì)算:
NuRE=(1-Nusen/Nugr)×100%
(1)
其中,Nusen和Nugr表示單位生物量中衰老器官(如衰老葉)和幼嫩器官(如新葉)的養(yǎng)分濃度。在各種各樣關(guān)于養(yǎng)分重吸收的研究中(大部分?jǐn)?shù)據(jù)來(lái)自美國(guó)和歐洲的森林生態(tài)系統(tǒng))發(fā)現(xiàn),葉片氮重吸收效率(nitrogen resorption efficiency,NRE)和磷重吸收率(phosphorus resorption efficiency,PRE)分別為50%(n=287)和52%(n=226)[4],而通過(guò)meta分析,在覆蓋了全球31個(gè)國(guó)家(大部分?jǐn)?shù)據(jù)來(lái)自歐洲、北美、俄羅斯和非洲)關(guān)于陸生植物養(yǎng)分重吸收的86個(gè)研究中發(fā)現(xiàn),NRE和PRE的平均值分別為62.1%和64.9%[9]。這主要是因?yàn)閂ergutz等[9]考慮了葉片衰老時(shí)發(fā)生的質(zhì)量損失,而這部分損失會(huì)使養(yǎng)分重吸收效率低估約10%[17]。
考慮到葉片衰老過(guò)程中質(zhì)量的損失,使用校正后的公式:
NuRE=(1-Nusen/Nugr×MLCF)×100%
(2)
其中,MLCF為質(zhì)量損失校正因子(mass loss correction factor),一般為老葉與新葉的干重比,或者當(dāng)葉片質(zhì)量損失率(leaf mass loss, LML)有效時(shí),由1-LML/100 估算。不同生長(zhǎng)類(lèi)型植物的MLCF值不同,因?yàn)橹参锶~片的養(yǎng)分濃度通過(guò)質(zhì)量和面積來(lái)表達(dá),質(zhì)量濃度不能計(jì)算在衰老過(guò)程中因葉片生物量的減少而引起的葉片可溶性碳和非目標(biāo)元素的變化,從而引起重吸收的變化;而隨著衰老植物葉片面積縮小,也會(huì)改變重吸收的大小[17-18],相比之下,以葉片面積為基準(zhǔn)得到的重吸收效率則較高[19]。根據(jù)大量數(shù)據(jù)分析表明,LML平均值為(24.2±2.1),則MLCF的平均值在0.737與0.779之間[9,17]。然而現(xiàn)有研究中,用到校正公式的情況很少[9,17],因?yàn)橹匚找矔?huì)導(dǎo)致葉片物質(zhì)減少和厚度減小,而且在成年階段表現(xiàn)更突出,而葉片物質(zhì)減少又會(huì)導(dǎo)致低估重吸收效率[20],因而這是一個(gè)相互影響的過(guò)程。
植物養(yǎng)分重吸收能力大小也可以用養(yǎng)分重吸收度(nutrient resorption proficiency,NuRP)[5]來(lái)表征。NuRP是指植物衰老葉片中養(yǎng)分濃度能夠減少到的最低水平,可以用養(yǎng)分轉(zhuǎn)移后衰老組織中的最低養(yǎng)分濃度來(lái)表示,養(yǎng)分濃度越低表明重吸收度越高[5,21]。根據(jù)多年生木本植物衰老葉片養(yǎng)分濃度大小,養(yǎng)分重吸收度可分為完全重吸收(complete resorption)和不完全重吸收(incomplete resorption),其中衰老葉中氮濃度低于7.0 mg·g-1,落葉植物和常綠植物磷濃度分別低于0.5和0.4 mg·g-1被視為完全重吸收,而二者分別大于10.0和0.8 mg·g-1被視為不完全重吸收[5]。養(yǎng)分重吸收度比養(yǎng)分重吸收效率更能直接表征養(yǎng)分重吸收的強(qiáng)度,因?yàn)轲B(yǎng)分重吸收度不受綠葉取樣時(shí)間和空間的影響[5]。NuRP直接影響了凋落物的質(zhì)量,凋落物的分解速率以及土壤的速效養(yǎng)分[5,16,22]。衰老葉片中的養(yǎng)分濃度越低,表明從衰老葉片中轉(zhuǎn)移到幼嫩組織的養(yǎng)分越多,增加了養(yǎng)分在植物體內(nèi)的留存時(shí)間,同時(shí)使得凋落物分解時(shí)的養(yǎng)分淋溶量減少,從而減緩養(yǎng)分從整個(gè)系統(tǒng)的損失[23]。
植物養(yǎng)分重吸收受內(nèi)稟遺傳特性控制,不同物種間的重吸收差異很明顯。這不僅與特定物種的養(yǎng)分需求、植物對(duì)養(yǎng)分組分的權(quán)衡(如N∶P)[24-25]、吸收能力等有關(guān),還可能受植物本身調(diào)節(jié)物質(zhì)轉(zhuǎn)移的內(nèi)源因子影響,如庫(kù)容大小[26-27]、韌皮部轉(zhuǎn)運(yùn)率[20,28]、葉片的結(jié)構(gòu)性防御力[29]、葉片脫落動(dòng)態(tài)[30-31]等的影響。
不同類(lèi)型植物間葉片養(yǎng)分重吸收有明顯差異[32-33]。通過(guò)對(duì)大部分來(lái)自美國(guó)和歐洲的養(yǎng)分重吸收綜合分析發(fā)現(xiàn),常綠樹(shù)、落葉樹(shù)、禾本科和非禾本科草本植物的NRE分別為33%~82%、55%~83%、28%~78%和40%~81%,PRE分別為25%~98%、45%~81%、34%~92%和62%~88%[4],但常綠植物和落葉植物類(lèi)型間重吸收可能無(wú)差異[3]。在養(yǎng)分完全重吸收后,落葉樹(shù)的N重吸收度(nitrogen resorption proficiency,NRP,實(shí)際應(yīng)該是衰老葉片N濃度)為<7.0 mg·g-1、P重吸收度(phosphorus resorption proficiency,PRP,實(shí)際應(yīng)該是衰老葉片P濃度)為<0.5 mg·g-1,而常綠樹(shù)的PRP為<0.4 mg·g-1[5]。對(duì)中國(guó)北方6種森林類(lèi)型137種木本植物研究發(fā)現(xiàn),喬木NRE和PRE均顯著高于灌木,針葉樹(shù)高于闊葉樹(shù)[34]。有研究表明,NRE的大小可表現(xiàn)為禾本科>非禾本科>灌木[35]。在全球尺度上,NRE表現(xiàn)為禾草類(lèi)>非禾草類(lèi)>松柏類(lèi)>落葉植物>蕨類(lèi)植物>常綠植物,PRE表現(xiàn)為禾草類(lèi)>松柏類(lèi)>非禾草類(lèi)>蕨類(lèi)>落葉植物>常綠植物[9]。
研究表明,固氮物種NRE大大低于非固氮物種[5],而PRE則較高[34]。段兵紅等[36]結(jié)果顯示,紫花苜蓿(Medicagosativa)葉片NRE和PRE的均值低于已經(jīng)報(bào)道的50%和52%[4]或者62%和65%[9]。也有特例發(fā)現(xiàn),山龍眼科植物斑克木(Banksiaintegrifolia)PRE遠(yuǎn)高于豆科植物金合歡(Acaciafarnesiana)[37]。每個(gè)物種只是反映了在當(dāng)前環(huán)境條件下的實(shí)際重吸收效率值,并不能反映該植物在任意條件下的最大重吸收值[8,37]。同一物種在不同地區(qū)的重吸收值不同是因?yàn)槭艿搅怂钟行?、衰老時(shí)長(zhǎng)、葉片養(yǎng)分情況和遮陰等多種因素的影響[5,9]。
施肥實(shí)驗(yàn)[6,22,38]和沿自然養(yǎng)分梯度的觀測(cè)[39-41]均表明,低養(yǎng)分地區(qū)的植物NuRE和NuRP較高[5,42-43],而高養(yǎng)分供應(yīng)下則較低[6,10,41,44]。雖然生長(zhǎng)較慢,但是養(yǎng)分物質(zhì)損失率低的物種在養(yǎng)分貧乏生境中將占優(yōu)勢(shì),而生長(zhǎng)較快、養(yǎng)分物質(zhì)損失速率高的物種則在養(yǎng)分充足生境中占優(yōu)勢(shì)[45-46]。對(duì)生長(zhǎng)于迥異生境下的多年生草本植物而言,在恒定養(yǎng)分供給水平下,處于最適生境條件下物種的N素利用效率先隨養(yǎng)分有效性提高而增大,而當(dāng)養(yǎng)分有效性增加到一定水平后,N素利用效率又開(kāi)始下降[47],這可能意味著吸收到體內(nèi)的N素再次利用減少了[48]。此外,貧瘠生境,低生產(chǎn)力的物種葉片中所觀察到的高濃度酚醛樹(shù)脂可能會(huì)造成蛋白質(zhì)合成之前發(fā)生蛋白質(zhì)沉降現(xiàn)象,而這種現(xiàn)象會(huì)通過(guò)降低養(yǎng)分重吸收作用而使養(yǎng)分利用率降低[2,20,45]。因此,養(yǎng)分貧瘠樣地中的物種未必是由于具有高養(yǎng)分利用效率才能適應(yīng)貧瘠環(huán)境,更多地可能是由于具有低養(yǎng)分損失率而適應(yīng)貧瘠環(huán)境。
養(yǎng)分重吸收隨土壤養(yǎng)分有效性加強(qiáng)而降低。一般地,NuRE隨土壤養(yǎng)分供應(yīng)的增加而降低[6,35,38,49-52],NuRP也隨土壤養(yǎng)分供應(yīng)的增加而減小[42,50,53-55],意味著衰老葉養(yǎng)分濃度隨土壤速效養(yǎng)分的增加而相應(yīng)增加了。如Enoki等[56]發(fā)現(xiàn),日本滋賀縣黑松(Pinusthunbergii)葉片NRE隨著土壤N有效性的降低從43%提高到77%。又如Vourlitis等[57]發(fā)現(xiàn),巴西薩王那地區(qū),NRP隨土壤全N的減少而升高,PRP和PRE隨土壤可提取P的減少而升高。此外,與NuRE相比,葉片NuRP與土壤養(yǎng)分有效性的關(guān)系更為密切[6,13,42,53-54,57]。
在農(nóng)業(yè)系統(tǒng)中,施肥能改善土壤養(yǎng)分供應(yīng),提高土壤養(yǎng)分有效性,極大地提高作物的生產(chǎn)性能。但是,施肥如何影響?zhàn)B分重吸收尚無(wú)一致的結(jié)論。如Aerts[4]對(duì)60個(gè)物種的施肥試驗(yàn)數(shù)據(jù)進(jìn)行總結(jié),發(fā)現(xiàn)其中63%的物種NuRE對(duì)施肥沒(méi)有響應(yīng),而Son等[58]的研究表明,施肥(N和P)可使日本落葉松(Japaneselarch)NRE提高。土壤高N無(wú)P的控制條件下,P重吸收加強(qiáng);僅N添加可能導(dǎo)致P成為次生限制性養(yǎng)分[59]。淡水濕地中,N添加降低了小葉章(Deyeuxiaangustifolia)葉片的NRE、PRE、NRP和PRP,導(dǎo)致凋落物中的N和P濃度較高[16]。因而土壤養(yǎng)分供應(yīng)與NuRE間尚沒(méi)有完全一致的關(guān)系[6,22,28,30,49,51,60-62]。施肥可能會(huì)改變土壤中其他養(yǎng)分的含量,間接影響土壤水分、熱量以及微生物活性[52],從而最終多途徑調(diào)控養(yǎng)分重吸收。因此,在實(shí)踐中,通過(guò)施肥管理措施調(diào)控養(yǎng)分重吸收的難度很大,還需要深入研究,以更好地指導(dǎo)生產(chǎn)。
土壤水分不僅是影響土壤養(yǎng)分有效性的關(guān)鍵因素,也是影響陸地生態(tài)系統(tǒng)養(yǎng)分循環(huán)進(jìn)程的關(guān)鍵因素[63]。它影響了土壤的氮礦化速率、礦質(zhì)氮的移動(dòng)和微生物活性[51,63-64],從而改變了植物養(yǎng)分的吸收和積累模式,最終改變了養(yǎng)分重吸收[4-5]。一般的,植物NuRE與植物的水分利用效率呈顯著的負(fù)相關(guān)關(guān)系[65],但不同的養(yǎng)分元素對(duì)土壤水分的響應(yīng)不一致,如土壤水分增多可導(dǎo)致NRE降低,而對(duì)P重吸收沒(méi)有顯著影響[51]。干旱會(huì)導(dǎo)致葉片出現(xiàn)健康存活、干燥死亡、干旱誘導(dǎo)衰老(表現(xiàn)為失綠)、正常衰老(常在秋季)等幾種狀態(tài),葉片衰老方式不同的樹(shù)種,養(yǎng)分重吸收強(qiáng)度也存在差異。干旱誘導(dǎo)落葉型植物NRP和PRP比其他植物的更高(即重吸收更完全)[66]。土壤水分狀況通過(guò)調(diào)節(jié)土壤養(yǎng)分有效性而影響植物NuRE,在維持養(yǎng)分循環(huán)中扮演非常重要的角色[63-64]。因此,合理控水,對(duì)于減少成本,提高養(yǎng)分重吸收,從而提高生產(chǎn)力具有重要意義。
光照能影響植物葉片的光合作用,從而影響氣孔的開(kāi)閉、蒸騰等,最終對(duì)根系吸收養(yǎng)分的能力產(chǎn)生影響。有效光的改變可能會(huì)引起植物幼苗的養(yǎng)分循環(huán)組分和NRE的變化[67]。實(shí)施突然遮陰會(huì)減小樺樹(shù)(Alaskan)的NRE[11,28],這種影響對(duì)長(zhǎng)期生長(zhǎng)在陰影下的植物不明顯[68]。耐陰植物的NuRE低于需光植物,因此,單位面積的枯葉中氮濃度更高[69],對(duì)應(yīng)的NuRP更低。遮陰下植物衰老葉片中的N 和P的含量較高,從而導(dǎo)致對(duì)應(yīng)元素的NuRE比對(duì)照低[11]。但是,對(duì)葡萄牙櫟(Quercusfaginea)而言,適度的遮陰下NRE最大,而全光照下NRE最小[67],強(qiáng)光處理下的挪威槭(Acerplatanoides)和糖槭(Acersaccharum)幼苗比適宜光照處理下的NRE分別高42%和36%[70]。也有研究表明,當(dāng)植物沒(méi)有光合作用時(shí),仍具有重吸收作用,但是植物不可能重吸收枯葉中所有的氮,如,細(xì)胞壁上嵌入的蛋白質(zhì)不會(huì)從枯葉中轉(zhuǎn)移[68]。因此,植物在不同光照下養(yǎng)分重吸收的差異,不僅受到光強(qiáng)的影響,也可能與植物本身對(duì)光的響應(yīng)有關(guān)。
溫度是影響植物生長(zhǎng)的重要因素之一,每種植物都有其自身適宜生長(zhǎng)的溫度。環(huán)境溫度的變化可調(diào)節(jié)根系酶活力,影響植物養(yǎng)分吸收,因而導(dǎo)致養(yǎng)分重吸收發(fā)生變化。研究表明,夏季溫度對(duì)NRE具有顯著的影響,并表現(xiàn)出顯著負(fù)相關(guān)性[71]。高溫脅迫導(dǎo)致活性氧清除能力降低,使葉片中活性氧大量產(chǎn)生,從而加劇葉片細(xì)胞的膜脂過(guò)氧化程度,加速葉片的衰老[72];同時(shí),高溫也會(huì)使小麥(Triticumaestivum)的劍葉丙二醛含量升高,超氧化物歧化酶活性和可溶性蛋白質(zhì)含量降低,加速植株衰老[73],從而使得養(yǎng)分來(lái)不及轉(zhuǎn)移而留存在衰老葉片中,降低重吸收能力。
植物體內(nèi)的氮和磷不僅受到非生物因素的影響,而且隨著植物的生長(zhǎng)發(fā)育發(fā)生變化[52]。在植物的整個(gè)生長(zhǎng)階段中,不同時(shí)期對(duì)養(yǎng)分的需求有所差異,因而對(duì)養(yǎng)分的敏感程度和吸收能力也各不相同,從而表現(xiàn)出不同養(yǎng)分重吸收特征。養(yǎng)分重吸收在生殖結(jié)構(gòu)形成時(shí)增加,移除時(shí)降低[28,39]。在溫帶地區(qū),進(jìn)行生殖生長(zhǎng)的植物個(gè)體葉片養(yǎng)分含量低于進(jìn)行營(yíng)養(yǎng)生長(zhǎng)的個(gè)體葉片養(yǎng)分含量,表明生殖生長(zhǎng)狀態(tài)會(huì)極大地影響?zhàn)B分分配,包括重吸收這一養(yǎng)分循環(huán)的重要環(huán)節(jié)[41,74-75]??赡苁浅赡觌A段新葉片的出現(xiàn)很快(一波),常伴隨成花,對(duì)養(yǎng)分需求大且快,土壤供應(yīng)不及,則重吸收發(fā)揮作用[19]。短期或長(zhǎng)期生殖需求較大的樹(shù)木比生殖需求較小的樹(shù)木具有更低的枯葉氮磷含量,表明NuRP增大[41]。此外,相比幼苗而言,成年植株的葉片NRE較高(綠葉N濃度也較高),但是NRP無(wú)差異。相比成年階段,早期階段的綠色葉片N濃度和光合養(yǎng)分利用率較低[76]。同時(shí),早期階段綠色葉片單位面積N含量與NRE正相關(guān);成年階段則不存在[19]??赡苁窃谠缙陔A段快速生長(zhǎng)導(dǎo)致的組織(如葉片)N和P濃度的減小,但在后期因?yàn)樯L(zhǎng)暫緩而得到補(bǔ)充或因養(yǎng)分重吸收的啟動(dòng)而補(bǔ)充[77]。
植物葉片的壽命長(zhǎng)短對(duì)葉片的養(yǎng)分重吸收也具有影響。一般地,長(zhǎng)壽命葉片NuRE比短壽命葉片更高[3,78]。因此,植物葉片的壽命越長(zhǎng),保持的葉片生物量越大,植物從衰老葉中轉(zhuǎn)移的養(yǎng)分就越多,從而使其在氣溫回升、土溫仍然較低的時(shí)期能維持正常生長(zhǎng)[79]。同時(shí),葉片滯留于植物體上的時(shí)間更長(zhǎng),養(yǎng)分利用效率也就越大。然而,也有研究表明,葉片衰老持續(xù)時(shí)間較長(zhǎng)的物種(如云杉Piceaasperata和冷杉Abiesfabri)NuRE較低,而葉片脫落持續(xù)時(shí)間較短的物種(如落葉松Larixdecidua)NuRE較高[30,79]。也有研究發(fā)現(xiàn)生長(zhǎng)早期植物往往追求較高的光合同化,中午水勢(shì)較低[80],從而提早了葉片的死亡,導(dǎo)致養(yǎng)分重吸收降低。此外,Chapin等[28]研究發(fā)現(xiàn),延長(zhǎng)葉片在樹(shù)上的生長(zhǎng)時(shí)間對(duì)NRE、PRE沒(méi)有影響。
除了葉片壽命以外,植物自身的壽命對(duì)其養(yǎng)分利用也有重要影響。一般地,長(zhǎng)壽命植物的葉片通常具有較小養(yǎng)分濃度,其較高NuRE可減少養(yǎng)分損失[3],從而有助于植物的適應(yīng)和生存。然而,對(duì)于壽命較長(zhǎng)物種而言,不同年齡時(shí)的養(yǎng)分供應(yīng)、吸收能力等也有差異,因而,養(yǎng)分重吸收不同。一般地,老齡或成齡植株NRE、PRE高于幼齡[80-81]。但是,也有研究表明,植物NRE和PRE隨年齡增大先升高后降低[25,82-83]。此外,植物NuRE也可能隨年齡增加而降低[23,84]。這種養(yǎng)分保存能力的降低,表明隨著年齡的增加,植物對(duì)生境的適應(yīng)性逐漸降低,在對(duì)養(yǎng)分的保存上出現(xiàn)了衰退,從而直接導(dǎo)致重吸收功能減弱,使得養(yǎng)分重吸收與年齡的關(guān)系更為復(fù)雜。
葉片的衰老過(guò)程與源葉同化物的供應(yīng)及源的大小(葉面積)有關(guān)[85]。影響植物從衰老葉片內(nèi)轉(zhuǎn)移養(yǎng)分的主要原因并不是土壤肥力而是植物養(yǎng)分轉(zhuǎn)移中的“源-庫(kù)”關(guān)系,即養(yǎng)分從衰老葉片(“源”)中轉(zhuǎn)移到活躍組織(“庫(kù)”)的過(guò)程,同時(shí),植物體內(nèi)(尤其葉片)養(yǎng)分濃度的變化可能是養(yǎng)分重吸收變化的直接原因,轉(zhuǎn)移養(yǎng)分?jǐn)?shù)量的多少比植物本身的養(yǎng)分狀態(tài)及土壤養(yǎng)分有效性更為重要[86],但是目前對(duì)于葉片養(yǎng)分濃度的變化與重吸收變化的關(guān)系并沒(méi)有一致的結(jié)論,既表現(xiàn)出正相關(guān)[32],又表現(xiàn)出負(fù)相關(guān)[9,18,87-88]和無(wú)關(guān)[33]。但是,也有研究表明,加強(qiáng)“庫(kù)”(對(duì)麥穗進(jìn)行遮陰)或減弱“源”(摘去第一片葉)都能提高養(yǎng)分的內(nèi)遷移效率,因而源-庫(kù)關(guān)系理論在重吸收調(diào)控中并不完全發(fā)揮作用[89]。
衰老是植物生長(zhǎng)發(fā)育、形態(tài)建成和對(duì)環(huán)境應(yīng)答反應(yīng)中一個(gè)重要的生理現(xiàn)象,伴隨一系列生理變化和分子事件,是一個(gè)受內(nèi)外因子直接或間接影響的、高度有序的細(xì)胞程序化死亡過(guò)程[90-92]。在衰老的葉片細(xì)胞中,經(jīng)過(guò)高度有序地去組裝和降解過(guò)程,代謝產(chǎn)物(如營(yíng)養(yǎng)物質(zhì))又會(huì)被重新運(yùn)輸?shù)礁贻p或再生器官中[93-95]。因此,養(yǎng)分重吸收與衰老密切聯(lián)系。Nooden等[96]提出三段式理論,將葉片衰老分為3個(gè)階段,即起始(initiation)、衰退(degeneration)和終末(terminal)。外界環(huán)境信號(hào)和內(nèi)源發(fā)育信號(hào)共同作用誘發(fā)葉片衰老,首先會(huì)使得葉片的光合作用下降,源-庫(kù)關(guān)系轉(zhuǎn)變,幼葉作為“庫(kù)”器官直到成熟,而老葉作為“源”器官提供糖類(lèi);當(dāng)幼葉發(fā)育成熟,光合作用達(dá)到最大,其對(duì)糖的需求量開(kāi)始降低,有限的需求量將導(dǎo)致老葉中糖的積累,并誘導(dǎo)老葉的衰老[97-98]。其次細(xì)胞組分去組裝、大分子物質(zhì)降解,從而使得降解的產(chǎn)物作為營(yíng)養(yǎng)物質(zhì)被重新運(yùn)送到“庫(kù)”器官;在大分子降解過(guò)程中,各種蛋白降解系統(tǒng)和脂類(lèi)降解系統(tǒng)也被激活,營(yíng)養(yǎng)物質(zhì)會(huì)被重新利用,從而促進(jìn)衰老[94,99]。最后細(xì)胞死亡,葉片脫落[95]。
隨著葉片的逐漸衰老,有機(jī)氮和磷被水解,在葉片脫落前無(wú)機(jī)磷和氨基酸態(tài)氮被轉(zhuǎn)移出衰老葉片[20]。隨著衰老,葉片中被重吸收的磷占核酸和磷脂水解化合物全磷含量的40%~47%,被重吸收的氮占蛋白質(zhì)水解及后續(xù)的氨基酸再轉(zhuǎn)移氮的82%~91%[20]。
養(yǎng)分重吸收是植物“獲取”養(yǎng)分的重要途徑。除了葉片之外,植物的其他組織器官也可以進(jìn)行養(yǎng)分重吸收,包括細(xì)莖、樹(shù)木的芯材和能夠儲(chǔ)存養(yǎng)分的根等[100-101]。葉片養(yǎng)分重吸收在過(guò)去的40多年間已經(jīng)被廣泛研究,但是關(guān)于莖和根養(yǎng)分重吸收的研究卻很少。研究表明,在植物非葉片器官中,莖稈的重吸收較其他器官高,且在植物養(yǎng)分經(jīng)濟(jì)和生態(tài)系統(tǒng)養(yǎng)分循環(huán)中扮演重要角色[13,102]。莖與植物其他組織相比,最大不同點(diǎn)在于衰老速度特別慢[100],可能導(dǎo)致其重吸收較大。也有研究表明,中國(guó)杉的葉片NRE大于細(xì)枝[103]。另外,植物細(xì)根和老根間的養(yǎng)分含量幾乎沒(méi)有差異[26,104-105],表明根的養(yǎng)分重吸收與葉片或其他組織相比是可以忽略的[106-107]。在養(yǎng)分重吸收過(guò)程中,根不僅是庫(kù)也是源;同樣地,莖既是養(yǎng)分從葉片重吸收后的庫(kù),又是營(yíng)養(yǎng)生長(zhǎng)和生殖生長(zhǎng)的源[20,26,107-108]。因此,與葉片相比,植物其他組織(莖、根、葉鞘等)養(yǎng)分重吸收更為復(fù)雜,相關(guān)研究較少[101]。
目前,在全球尺度上,植物葉片的養(yǎng)分重吸收強(qiáng)度,已經(jīng)有一些明確的閾值范圍,而其他器官(如莖稈和根)的養(yǎng)分重吸收強(qiáng)度,則尚不確定。
植物一旦開(kāi)始衰老,大量養(yǎng)分會(huì)從植物的衰老部分通過(guò)韌皮部轉(zhuǎn)移到正在生長(zhǎng)的庫(kù)中,如種子[46]。在營(yíng)養(yǎng)生長(zhǎng)階段,衰老器官將養(yǎng)分轉(zhuǎn)運(yùn)到植物幼嫩部分[109];在生殖生長(zhǎng)階段,隨著整個(gè)衰老過(guò)程開(kāi)始,母本植物的所有組織和器官死亡,養(yǎng)分從衰老組織重新轉(zhuǎn)移到種子中[110]。但是,植物的養(yǎng)分重吸收過(guò)程與衰老的關(guān)系尚不明確,需作進(jìn)一步的研究。
植物養(yǎng)分重吸收過(guò)程受多種因子的調(diào)節(jié),在不同的物種、不同組織中表現(xiàn)出不同的模式和反應(yīng)。應(yīng)加強(qiáng)對(duì)控制條件下重吸收規(guī)律的研究,深入了解其調(diào)控機(jī)制,在實(shí)踐中結(jié)合水肥管理等措施來(lái)調(diào)節(jié)植物養(yǎng)分重吸收,從而提高植物(作物)的適應(yīng)性和生產(chǎn)性能。
此外,還可根據(jù)需求,選擇特定重吸收強(qiáng)度的作物(如牧草),充分利用其重吸收特性,保證產(chǎn)量和品質(zhì)。
參考文獻(xiàn)References:
[1] Killingbeck K T. The terminological jungle revisited-making a case for use of the term resorption. Oikos, 1986, 46(2): 263-264.
[2] Aerts R, de Caluwe H. Nutritional and plant-mediated controls on leaf litter decomposition ofCarexspecies. Ecology, 1997, 78(1): 244-260.
[3] Aerts R, Chapin F S. The mineral nutrition of wild plants revisited: A re-evaluation of processes and patterns. Advances in Ecological Research, 2000, 30: 1-67.
[4] Aerts R. Nutrient resorption from senescing leaves of perennials: Are there general patterns. Journal of Ecology, 1996, 84(4): 597-608.
[5] Killingbeck K T. Nutrients in senesced leaves: Keys to the search for potential resorption and resorption proficiency. Ecology, 1996, 77(6): 1716-1727.
[6] Van Heerwaarden L M, Toet S, Aerts R. Nitrogen and phosphorus resorption efficiency and proficiency in six sub-arctic bog species after 4 years of nitrogen fertilization. Journal of Ecology, 2003, 91(6): 1060-1070.
[7] Covelo F, Rodríguez A, Gallardo A. Spatial pattern and scale of leaf N and P resorption efficiency and proficiency in aQuercusroburpopulation. Plant and Soil, 2008, 311(1/2): 109-119.
[8] Reed S C, Townsend A R, Davidson E A,etal. Stoichiometric patterns in foliar nutrient resorption across multiple scales. New Phytologist, 2012, 196(1): 173-180.
[9] Vergutz L, Manzoni S, Porporato A,etal. Global resorption efficiencies and concentrations of carbon and nutrients in leaves of terrestrial plants. Ecological Monographs, 2012, 82(2): 205-220.
[10] Zhao Q, Liu X Y, Hu Y L,etal. Effects of nitrogen addition on nutrient allocation and nutrient resorpiton efficiency inLarixgmelinii. Scientia Silvae Sinicae, 2010, 46(5): 14-19.
趙瓊, 劉興宇, 胡亞林,等. 氮添加對(duì)興安落葉松養(yǎng)分分配和再吸收效率的影響. 林業(yè)科學(xué), 2010, 46(5): 14-19.
[11] May J D, Killingbeck K T. Effects of preventing nutrient resorption on plant fitness and foliar nutrient dynamics. Ecology, 1992, 73: 1868-1878.
[12] Blanco J A, Imbert J B, Castillo F J. Thinning affects nutrient resorption and nutrient-use efficiency in twoPinussylvestrisstands in the Pyrenees. Ecological Applications, 2009, 19(3): 682-698.
[13] Lü X T, Freschet G T, Flynn D F B,etal. Plasticity in leaf and stem nutrient resorption proficiency potentially reinforces plant-soil feedbacks and microscale heterogeneity in a semi-arid grassland. Journal of Ecology, 2012, 100(1): 144-150.
[14] Veneklaas E J, Lambers H, Bragg J,etal. Opportunities for improving phosphorus use efficiency in crop plants. New Phytologist, 2012, 195(2): 306-320.
[15] Marschner P. Marschner’s mineral nutrition of higher plants (3rd edition). Amsterdam, Netherlands: Academic Press (Elsevier), 2012.
[16] Mao R, Song C C, Zhang X H,etal. Response of leaf, sheath and stem nutrient resorption to 7 years of N addition in freshwater wetland of Northeast China. Plant and Soil, 2013, 364(1/2): 385-394.
[17] Van Heerwaarden L M, Toet S, Aerts R. Current measures of nutrient resorption efficiency lead to a substantial underestimation of real resorption efficiency: Facts and solutions. Oikos, 2003, 101(3): 664-669.
[18] Kobe R K, Lepczyk C A, Iyer M. Resorption efficiency decreases with increasing green leaf nutrients in a global data set. Ecology, 2005, 86(10): 2780-2792.
[19] Mediavilla S, García-Iglesias J, González-Zurdo P,etal. Nitrogen resorption efficiency in mature trees and seedlings of four tree species co-occurring in a Mediterranean environment. Plant and Soil, 2014, 385(1/2): 205-215.
[20] Chapin F S, Kedrowski R A. Seasonal changes in nitrogen and phosphorus fractions and autumn retranslocation in evergreen and deciduous taiga trees. Ecology, 1983, 64(2): 376-391.
[21] Lü X T, Cui Q, Wang Q B,etal. Nutrient resorption response to fire and nitrogen addition in a semi-arid grassland. Ecological Engineering, 2011, 37(3): 534-538.
[22] Vitousek P M. Foliar and litter nutrients, nutrient resorption, and decomposition in HawaiianMetrosiderospolymorpha. Ecosystems, 1998, 1(4): 401-407.
[23] Zeng D H, Chen G S, Chen F S,etal. Foliar nutrients and their resorption efficiencies in fourPinussylvestrisvar. mongolica plantations of different ages on sandy soil. Scientia Silvae Sinicae, 2005, 41(5): 21-27.
曾德慧, 陳廣生, 陳伏生, 等. 不同林齡樟子松葉片養(yǎng)分含量及其再吸收效率. 林業(yè)科學(xué), 2005, 41(5): 21-27.
[24] Sterner R W, Elser J J. Ecological stoichiometry: The biology of elements from molecules to the biosphere. Princeton, USA: Princeton University Press, 2002.
[25] Wang Z N, Lu J Y, Yang H M,etal. Resorption of nitrogen, phosphorus and potassium from leaves of lucerne stands of different ages. Plant and Soil, 2014, 383(1/2): 301-312.
[26] Nambiar E K S, Fife D N. Nutrient retranslocation in temperate conifers. Tree Physiology, 1991, 9(1/2): 185-207.
[27] Silla F, Escudero A. Uptake, demand and internal cycling of nitrogen in saplings ofMediterraneanquercusspecies. Oecologia, 2003, 136(1): 28-36.
[28] Chapin F S, Moilanen L. Nutritional controls over nitrogen and phosphorus resorption fromAlaskanbirchleaves. Ecology, 1991, 72(2): 709-715.
[29] Wright I J, Cannon K. Relationships between leaf lifespan and structural defences in a low-nutrient, sclerophyll flora. Functional Ecology, 2001, 15: 351-359.
[30] Del Arco J M, Escudero A, Garrido M V. Effects of site characteristics on nitrogen retranslocation from senescing leaves. Ecology, 1991, 72(2): 701-708.
[31] Escudero A, Del Arco J M, Sanz I C,etal. Effects of leaf longevity and retranslocation efficiency on the retention time of nutrients in the leaf biomass of different woody species. Oecologia, 1992, 90(1): 80-87.
[32] Diehl P, Mazzarino M J, Funes F,etal. Nutrient conservation strategies in native Andean-Patagonian forests. Journal of Vegetation Science, 2003, 14(1): 63-70.
[33] Cai Z Q, Bongers F. Contrasting nitrogen and phosphorus resorption efficiencies in trees and lianas from a tropical montane rain forest in Xishuangbanna, south-west China. Journal of Tropical Ecology, 2007, 23(1): 115-118.
[34] Tang L Y. Study on leaves nutrient absorption of woody plant. Beijing: Beijing University, 2012.
湯璐瑛. 木本植物葉片養(yǎng)分重吸收研究. 北京: 北京大學(xué), 2012.
[35] Zhang J H, Li H, Shen H H,etal. Effects of nitrogen addition on nitrogen resorption in temperate shrublands in northern China. PloS One, 2015, 10(6): e0130434.
[36] Duan B H, Lu J Y, Liu M G,etal. Relationships between biological nitrogen fixation and leaf resorption of nitrogen, phosphorus, and potassium in the rain-fed region of eastern Gansu, China. Acta Prataculturae Sinica, 2016, 25(12): 76-83.
段兵紅, 陸姣云, 劉敏國(guó), 等. 隴東雨養(yǎng)農(nóng)區(qū)紫花苜蓿葉片氮、磷、鉀重吸收與生物固氮的偶聯(lián)關(guān)系. 草業(yè)學(xué)報(bào), 2016, 25(12): 76-83.
[37] de Campos M C, Pearse S J, Oliveira R S,etal. Downregulation of net phosphorus-uptake capacity is inversely related to leaf phosphorus-resorption proficiency in four species from a phosphorus-impoverished environment. Annals of Botany, 2013, 111(3): 445-454.
[38] Li X F, Zheng X B, Han S J,etal. Effects of nitrogen additions on nitrogen resorption and use efficiencies and foliar litterfall of six tree species in a mixed birch and poplar forest, northeastern China. Canadian Journal of Forest Research, 2010, 40(11): 2256-2261.
[39] Pugnaire F I, ChapinF S. Controls over nutrient resorption from leaves of evergreen Mediterranean species. Ecology, 1993, 74(1): 124-129.
[40] Eckstein R L, Karlsson P S, Weih M. Leaf life span and nutrient resorption as determinants of plant nutrient conservation in temperate-arctic regions. New Phytologist, 1999, 143(1): 177-189.
[41] Tully K L, Wood T E, Schwantes A M,etal. Soil nutrient availability and reproductive effort drive patterns in nutrient resorption inPentaclethramacroloba. Ecology, 2013, 94(4): 930-940.
[42] Wright I J, Westoby M. Nutrient concentration, resorption and lifespan: leaf traits of Australian sclerophyll species. Functional Ecology, 2003, 17(1): 10-19.
[43] Chen F S, Hu X F, Ge G. Leaf N: P stoichiometry and nutrient resorption efficiency ofOphiopogonjaponicusin Nanchang City. Acta Prataculturae Sinica, 2007, 16(4): 47-54.
陳伏生, 胡小飛, 葛剛. 城市地被植物麥冬葉片氮磷化學(xué)計(jì)量比和養(yǎng)分再吸收效率. 草業(yè)學(xué)報(bào), 2007, 16(4): 47-54.
[44] Lovelock C E, Feller I C, Ball M C,etal. Testing the growth rate vs. geochemical hypothesis for latitudinal variation in plant nutrients. Ecology Letters, 2007, 10(12): 1154-1163.
[45] Grime J P, Cornelissen J H C, Thompson K,etal. Evidence of a causal connection between anti-herbivore defence and the decomposition rate of leaves. Oikos, 1996, 77(3): 489-494.
[46] Xing X R, Han X G, Chen L Z. A review on research of plant nutrient use efficiency. Chinese Journal of Applied Ecology, 2000, 11(5): 785-790.
邢雪榮,韓興國(guó),陳靈芝. 植物養(yǎng)分利用效率研究綜述. 應(yīng)用生態(tài)學(xué)報(bào), 2000, 11(5): 785-790.
[47] Vázquez de Aldana B R, Berendse F. Nitrogen-use efficiency in six perennial grasses from contrasting habitats. Functional Ecology, 1997, 11(5): 619-626.
[48] Silver W L. Is nutrient availability related to plant nutrient use in humid tropical forests. Oecologia, 1994, 98(3/4): 336-343.
[49] Güsewell S. Nutrient resorption of wetland graminoids is related to the type of nutrient limitation. Functional Ecology, 2005, 19(2): 344-354.
[50] Kozovits A R, Bustamante M M C, Garofalo C R,etal. Nutrient resorption and patterns of litter production and decomposition in a neotropical savanna. Functional Ecology, 2007, 21(6): 1034-1043.
[51] Lü X T, Han X G. Nutrient resorption responses to water and nitrogen amendment in semi-arid grassland of Inner Mongolia, China. Plant and Soil, 2010, 327(1/2): 481-491.
[52] Lü X T, Reed S C, Yu Q,etal. Nutrient resorption helps drive intra-specific coupling of foliar nitrogen and phosphorus under nutrient-enriched conditions. Plant and Soil, 2015, 398(1/2): 111-120.
[53] Rejmankova E. Nutrient resorption in wetland macrophytes: comparison across several regions of different nutrient status. New Phytologist, 2005, 167(2): 471-482.
[54] Richardson S J, Peltzer D A, Allen R B,etal. Resorption proficiency along a chronosequence: Responses among communities and within species. Ecology, 2005, 86(1): 20-25.
[55] Norris M D, Reich P B. Modest enhancement of nitrogen conservation via retranslocation in response to gradients in N supply and leaf N status. Plant and Soil, 2009, 316(1/2): 193-204.
[56] Enoki T, Kawaguchi H. Nitrogen resorption from needles ofPinusthunbergiiParl. growing along a topographic gradient of soil nutrient availability. Ecological Research, 1999, 14(1): 1-8.
[57] Vourlitis G L, de Almeida L F, Lawrence S,etal. Nutrient resorption in tropical savanna forests and woodlands of central Brazil. Plant Ecology, 2014, 215(9): 963-975.
[58] Son Y, Lee I K, Ryu S R. Nitrogen and phosphorus dynamics in foliage and twig of pitch pine and Japanese larch plantations in relation to fertilization. Journal of Plant Nutrition, 2000, 23(5): 697-710.
[59] Agüero M L, Puntieri J, Mazzarino M J,etal. Seedling response ofNothofagusspecies to N and P: linking plant architecture to N/P ratio and resorption proficiency. Trees, 2014, 28(4): 1185-1195.
[60] Boerner R E J. Foliar nutrient dynamics and nutrient use efficiency of four deciduous tree species in relation to site fertility. Journal of Applied Ecology, 1984, 21(3): 1029-1040.
[61] Eckstein R L, Karlsson P S. Above-ground growth and nutrient use by plants in a subarctic environment: effects of habitat, life-form and species. Oikos, 1997, 79(2): 311-324.
[62] Soudzilovskaia N A, Onipchenko V G, Cornelissen J H C,etal. Effects of fertilisation and irrigation on ‘foliar afterlife’in alpine tundra. Journal of Vegetation Science, 2007, 18(5): 755-766.
[63] Liu P, Huang J H, Han X G,etal. Differential responses of litter decomposition to increased soil nutrients and water between two contrasting grassland plant species of Inner Mongolia, China. Applied Soil Ecology, 2006, 34(2/3): 266-275.
[64] Wang C H, Wan S, Xing X R,etal. Temperature and soil moisture interactively affected soil net N mineralization in temperate grassland in Northern China. Soil Biology and Biochemistry, 2006, 38(5): 1101-1110.
[65] Field C, Merino J, Mooney H A. Compromises between water-use efficiency and nitrogen-use efficiency in five species ofCaliforniaevergreens. Oecologia, 1983, 60(3): 384-389.
[66] Killingbeck K T. Can zinc influence nutrient resorption? A test with the drought-deciduous desert shrubFouquieriasplendens(ocotillo). Plant and Soil, 2008, 304(1/2): 145-155.
[67] Sanz-Pérez V, Castro-Díez P, Millard P. Effects of drought and shade on nitrogen cycling in the leaves and canopy ofMediterraneanquercusseedlings. Plant and Soil, 2009, 316(1/2): 45-56.
[68] Yasumura Y, Onoda Y, Hikosaka K,etal. Nitrogen resorption from leaves under different growth irradiance in three deciduous woody species. Plant Ecology, 2005, 178(1): 29-37.
[69] Lusk C H, Contreras O. Foliage area and crown nitrogen turnover in temperate rain forest juvenile trees of differing shade tolerance. Journal of Ecology, 1999, 87(6): 973-983.
[70] Duan B L, Paquette A, Juneau P,etal. Nitrogen resorption inAcerplatanoidesandAcersaccharum: influence of light exposure and leaf pigmentation. Acta Physiologiae Plantarum, 2014, 36(11): 3039-3050.
[71] Nordell K O, Karlsson P S. Resorption of nitrogen and dry matter prior to leaf abscission: variation among individuals, sites and years in the mountain birch. Functional Ecology, 1995, 9(2): 326-333.
[72] Liu H Z, Zheng F R, Zhao S J. Effects of heat- stress on the active oxygen-quenching system in leaf of wheat varieties with different senescence types. Guizhou Agricultural Sciences, 2006, 34(1): 8-10.
劉洪展, 鄭風(fēng)榮, 趙世杰. 高溫脅迫對(duì)不同衰老型小麥葉片中活性氧清除系統(tǒng)的影響. 貴州農(nóng)業(yè)科學(xué), 2006, 34(1): 8-10.
[73] Zhang L P, Jing Q, Dai T B,etal. Effects of temperature and illumination on flag leaf photosynthetic characteristics and senescence of wheat cultivars with different grain quality. Chinese Journal of Applied Ecology, 2008, 19(2): 311-316.
張黎萍, 荊奇, 戴廷波, 等. 溫度和光照強(qiáng)度對(duì)不同品質(zhì)類(lèi)型小麥旗葉光合特性和衰老的影響. 應(yīng)用生態(tài)學(xué)報(bào), 2008, 19(2): 311-316.
[74] Pakonen T, Laine K, Havas P,etal. Effects of berry production and deblossoming on growth, carbohydrates and nitrogen compounds inVacciniummyrtillusin north Finland. Acta Botanica Fennica, 1988, 136: 37-42.
[75] Cipollini M L, Stiles E W. Costs of reproduction inNyssasylvatica: sexual dimorphism in reproductive frequency and nutrient flux. Oecologia, 1991, 86(4): 585-593.
[76] Escudero A, Mediavilla S. Decline in photosynthetic nitrogen use efficiency with leaf age and nitrogen resorption as determinants of leaf life span. Journal of Ecology, 2003, 91(5): 880-889.
[77] Chapin F S, Schulze E D, Mooney H A. The ecology and economics of storage in plants. Annual Review of Ecology and Systematics, 1990, 21(1): 423-447.
[78] Huang J J, Wang X H, Yan E R. Leaf nutrient concentration, nutrient resorption and litter decomposition in an evergreen broad-leaved forest in eastern China. Forest Ecology and Management, 2007, 239(1/2/3): 150-158.
[79] Kimmins J P. Evaluation of consequences for future tree productivity of the loss of nutrients in whole-tree harvesting. Forest Ecology and Management, 1977, 1: 169-183.
[80] Mediavilla S, Escudero A. Stomatal responses to drought of mature trees and seedlings of two co-occurringMediterraneanoaks. Forest Ecology and Management, 2004, 187(2/3): 281-294.
[81] Liu B, Wang L H, Yin L M,etal. Seasonal variation and resorption characteristics of leaf N, P, and K in two agedXanthocerassorbifoliaplantations. Chinese Journal of Ecology, 2010, 29(7): 1270-1276.
劉波, 王力華, 陰黎明, 等. 兩種林齡文冠果葉N、P、K的季節(jié)變化及再吸收特征. 生態(tài)學(xué)雜志, 2010, 29(7): 1270-1276.
[82] Li R H, Wang S L, Wang Q K. Nutrient contents and resorption characteristics in needles of different agePinusmassoniana(Lamb.) before and after withering. Chinese Journal of Applied Ecology, 2008, 19(7): 1443-1447.
李榮華, 汪思龍, 王清奎. 不同林齡馬尾松針葉凋落前后養(yǎng)分含量及回收特征. 應(yīng)用生態(tài)學(xué)報(bào), 2008, 19(7): 1443-1447.
[83] Zhuang Y Z. Nutrients and their resorption efficiencies in leaves ofPinusmassonianaof different ages. Anhui Agricultural Science Bulletin, 2010, 16(18): 27-28, 52.
莊亞珍. 不同林齡馬尾松針葉養(yǎng)分含量及其再吸收效率. 安徽農(nóng)學(xué)通報(bào), 2010, 16(18): 27-28, 52.
[84] Deng H J, Chen A M, Yang S W,etal. Nutrient resorption efficiency and C∶N∶P stoichiometry in different ages ofLeucaenaleucocephal. Journal of Applied and Environmental Biology, 2015, 21(3): 522-527.
鄧浩俊, 陳愛(ài)民, 嚴(yán)思維, 等.不同林齡新銀合歡重吸收率及其C:N:P化學(xué)計(jì)量特征. 應(yīng)用與環(huán)境生物學(xué)報(bào), 2015, 21(3): 522-527.
[85] He P, Jin J Y, Lin B. Effects of nitrogen fertilizer on leaf senescence of spring maize and its mechanism. Scientia Agricultura Sinica, 1998, 31(3): 66-71.
何萍, 金繼運(yùn),林葆. 氮肥用量對(duì)春玉米葉片衰老的影響及其機(jī)理研究. 中國(guó)農(nóng)業(yè)科學(xué), 1998, 31(3): 66-71.
[86] Nambiar E K S. Do nutrients retranslocate from fine roots. Canadian Journal of Forest Research, 1987, 17(8): 913-918.
[87] Lajtha K. Nutrient reabsorption efficiency and the response to phosphorus fertilization in the desert shrubLarreatridentata(DC.) Cov. Biogeochemistry, 1987, 4(3): 265-276.
[88] Cté B, Fyles J W, Djalilvand H. Increasing N and P resorption efficiency and proficiency in northern deciduous hardwoods with decreasing foliar N and P concentrations. Annals of Forest Science, 2002, 59(3): 275-281.
[89] Pugnaire F I, Chapin F S. Environmental and physiological factors governing nutrient resorption efficiency in barley. Oecologia, 1992, 90(1): 120-126.
[90] Shen C G. Plant senescence physiology and molecular biology. Beijing: China Agriculture Press, 2001.
沈成國(guó). 植物衰老生理與分子生物學(xué). 北京: 中國(guó)農(nóng)業(yè)出版社, 2001.
[91] Wang X W, Cao H. Studies on mechanism of leaf senescence in high plant. Journal of Shanxi Agricultural University (Natural Science Edition), 2004, 24(4): 416-419.
王孝威, 曹慧. 高等植物衰老的機(jī)理研究. 山西農(nóng)業(yè)大學(xué)學(xué)報(bào)(自然科學(xué)版), 2004, 24(4): 416-419.
[92] Zhou F, Hua C, Wang R L. The leaf senescence and its regulation. Northern Horticulture, 2012, (1): 171-172.
周峰, 華春, 王仁雷. 植物葉片衰老及調(diào)控. 北方園藝, 2012, (1): 171-172.
[93] Himelblau E, Amasino R M. Nutrients mobilized from leaves ofArabidopsisthalianaduring leaf senescence. Journal of Plant Physiology, 2001, 158(10): 1317-1323.
[94] Li Q, Zhu Y X. The progress of plant senescence research and plant molecular breeding. Molecular Plant Breeding, 2003, 1(3): 289-296.
李晴, 朱玉賢. 植物衰老的研究進(jìn)展及其在分子育種中的應(yīng)用. 分子植物育種, 2003, 1(3): 289-296.
[95] Yan W Y, Ye S H, Dong Y J,etal. Research progress related to plant leaf senescence. Crops, 2010, (4): 4-9.
嚴(yán)雯奕, 葉勝海, 董彥君, 等. 植物葉片衰老相關(guān)研究進(jìn)展. 作物雜志, 2010, (4): 4-9.
[96] Nooden L D, Guiamet J J, John I. Senescence mechanisms. Physiologia Plantarum, 1997, 101(4): 746-753.
[97] Yoshida S. Molecular regulation of leaf senescence. Current Opinion Plant Biology, 2003, 6(1): 79-84.
[98] Ono K, Nishi Y, Watanabe A,etal. Possible mechanisms of adaptive leaf senescence. Plant Biology, 2001, 3(3): 234-243.
[99] Hellmann H, Estelle M. Plant development: Regulation by protein degradation. Science, 2002, 297: 793-797.
[100] Zhang J R. Effects of fertilization on leaf N and P resorption in an alpine meadow of the Tibetan Plateau. Lanzhou: Lanzhou University, 2016.
張晶然. 施肥對(duì)青藏高原高寒草甸植物葉片氮磷重吸收的影響. 蘭州: 蘭州大學(xué), 2016.
[101] Brant A N, Chen H Y H. Patterns and mechanisms of nutrient resorption in plants. Critical Reviews in Plant Sciences, 2015, 34(5): 471-486.
[102] Freschet G T, Aerts R, Cornelissen J H C. A plant economics spectrum of litter decomposability. Functional Ecology, 2012, 26(1): 56-65.
[103] Chen F S, Niklas K J, Liu Y,etal. Nitrogen and phosphorus additions alter nutrient dynamics but not resorption efficiencies of Chinese fir leaves and twigs differing in age. Tree Physiology, 2015, 35(10): 1106-1117.
[104] McClaugherty C A, Aber J D, Melillo J M. The role of fine roots in the organic matter and nitrogen budgets of two forested ecosystems. Ecology, 1982, 63(5): 1481-1490.
[105] Aerts R. Nutrient use efficiency in evergreen and deciduous species from heathlands. Oecologia, 1990, 84(3): 391-397.
[106] Gill R A, Jackson R B. Global patterns of root turnover for terrestrial ecosystems. New Phytologist, 2000, 147(1): 13-31.
[107] Gordon W S, Jackson R B. Nutrient concentrations in fine roots. Ecology, 2000, 81(1): 275-280.
[108] Milla R, Castro-Diez P, Maestro-Martinez M,etal. Relationships between phenology and the remobilization of nitrogen, phosphorus and potassium in branches of eight Mediterranean evergreens. New Phytologist, 2005, 168(1): 167-178.
[109] Gan S, Amasino R M. Making sense of senescence (Moleculargeneticregulation and manipulation of leaf senescence). Plant Physiology, 1997, 113(2): 313-319.
[110] Davies P J, Gan S. Towards an integrated view of monocarpic plant senescence. Russian Journal of Plant Physiology, 2012, 59(4): 467-478.