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Mechanisms and ecophysiological implications of foliar variegation in seedlings of Blastus cochinchinensis
calcium oxalate crystal
the maximum quantum yield of PSII
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|摘要:||Natural foliar variegation is common in the forest understory. Two main mechanisms of variegation, pigmental (chemical color) and structural (physical color), have been reported. Some plants maintain variegation throughout their lives, but some display this feature at the juvenile stage only. Blastus cochinchinensis (Melastomataceae) is a common understory shrub in Taiwan and East Asia, with two types of seedlings, variegated seedlings and normal green seedlings (non-variegated). The variegated leaves display novel and strong variegated patterns on their adaxial surfaces, consisting of series of white spots or chains on a normal green leaf. The aims of this study are to reveal the mechanism of this remarkable variegation and its effects on ecophysiology in seedlings of B. cochinchinensis, and with field surveys to gain understanding of its adaptive significance by correlating variegation and herbivore damage. In addition, Sonerila heterostemon, a plant collected from Singapore also with a strong variegation pattern before flowering, is studied to better understand the variegated mechanism of Melastomataceae.
The results attribute the variegation of B. cochinchinensis and S. heterostemon to at least three combined mechanisms including epidermal type, intercellular air space type and partial chlorophyll type. The adaxial epidermal cells of the white area of a variegated leaves are flate, and the adaxial epidermal cells of the green area of a variegated leaves and the normal green leaves are apophysis. The white area of a variegated leaves are thicker and have intercellular spaces between the adaxial epidermal cells and the upper mesophyll; the the green area of a variegated leaves and the normal green leaves are in tight contant with adaxial epidermal cells. The chloroplasts were fewer and smaller in the upper mesophyll, but their sizes were significantly larger in the lower mesophyll of the white area than the green area. The chloroplast ultrastructure, showing dense thylakoid membranes, shows no differences between the white area, the green area of a variegated leaf and the normal green leaf. Raphide-form oxalate crystals, which may increase light reflection and scattering, were found only in the adaxial epidermal cells of the white area of the variegated leaf of Blastus. Thus, a total of four variegation mechanisms were detected in the variegated leaf of Blastus, but it is unknown if this mechanism also occurs in Sonerila. In addition, the stomatal density on the abaxial leaf surface of the white area of Blastus was significantly lower than those of the green area and the normal green leaf. The normal green leaf has highest stomatal density.
The chlorophyll concentration of Blastus in the variegated leaves was lower than the green leaves. This may be related to the smaller size and lower number of chloroplasts in the upper mesophyll of the white area. The maximum quantum yield of PSII (Fv/Fm) of an area of variegated leaf covering both white and green areas was close to that of the green area alone. The maximum quantum yield of the green area was significantly higher than that of the normal green leaf. Under low light (300 μmol photons m-2 s-1), the PSII quantum yield and the electron transport rate (ETR) of the variegated leaf were lower than the normal green leaf, but the non-photochemical quenching (NPQ) of the variegated leaf was higher than the normal green leaf. The result implies that the variegated leaves of the variegated seedlings have photoprotection under the low light conditions where the seedlings of Blastus grow naturally in forests. At high light, the ETR of the variegated leaf was higher than the normal green leaf, but with lower NPQ and a similar PSII quantum yield to the normal green leaf. The net photosynthetic rate (Pn) of variegated leaves was significantly lower than that of green leaves.
Through twice repeated field surveys of 10 transects in the Huisun Forest Area and Lianhuachi Research Center, the percentage of variegated seedlings was found to be around 50% or more. Normal green leaves appear on average at the 8th node of the variegated seedling. Three types of variegation patterns were delineated: punctate, chain-like and lump, which consisted 1.5-24.8% leaf area. Such variegation patterns are extremely distinctive when viewed with the animal-eye specific imaging system (AESIS) to mimic the vision of honey bees. Notably, the herbivore damage in the variegated leaves was significantly lower than in the green leaves. One large multicellular trichome is located in the center of the white area of the variegated leaf, which may deter herbivores from landing and feeding. In addition, the density of glandular trichomes on the abaxial surface of the white area was significantly higher than those on the green area and the normal green leaves. No significant difference in the content of C%, N% and C/N ratio was found between the variegated leaf and the normal green leaf. Taken together, the striking variegated pattern, trichomes and crystals might contribute to the reduction of herbivore damage on the variegated leaf.
This is the first report of variegation caused by multiple combined mechanisms, with chemical, structural mechanisms and crystal effects. The micromorphological and structural differences of the variegated leaf lead to slightly weak the performance of photosynthesis of the variegated seedling, but it gains better photoprotection under low light, and significantly reduced herbivore damage. The variegated leaves appear only in the first seven pair leaves of the variegated seedling, showing an adaptive significance of heteroblasty. About half the seedlings of Blastus found in the forest edge of relatively open habitats are variegated, suggesting that this variegation trait is stabilized in Blastus and has evolutionary significance.|
植物自然斑葉（foliar variegation）形成的主要原因有兩大類，一與色素相關 （化學色）；另一則和葉片結構有關（物理色）。有趣的是許多具自然斑葉的植物大都生長在森林底層較陰暗潮濕的環境，有些植物終其一生都保有斑葉特性，而有些則僅在幼苗時期才有斑葉的發生。柏拉木（Blastus cochinchinensis，野牡丹科）為臺灣森林下層常見的灌木，其幼苗有些可表現搶眼而明顯的斑葉特徵。本研究旨在探討柏拉木幼苗斑葉形成的機制及其對生態生理的影響與植食性動物（herbivore）的交互作用。此外，亦搭配採集自新加坡的蜂鬥草屬植物Sonerila heterostemon，用於輔助探討野牡丹科（Melastomataceae）斑葉的機制。 結果顯示柏拉木與S. heterostemon斑葉白斑形成的原因，至少結合了表皮型、細胞間隙型與部分葉綠素缺乏型三種機制。斑葉白區的葉片較厚且表皮細胞較為平坦；斑葉綠區和一般綠葉的表皮細胞則具有較多的突起。斑葉白區的較近軸面表皮細胞與上層的葉肉細胞之間具有細胞間隙；斑葉綠區則與上層的葉肉細胞（漏斗狀細胞）緊密貼合。雖然斑葉白區的上層葉肉細胞內具較少而小的葉綠體，但其下層海綿組織細胞的葉綠體則顯著較大，可能可藉以補償。在斑葉白區、斑葉綠區（斑葉幼苗）和一般綠葉（綠葉幼苗）的葉綠體均具發達的類囊膜，三者之間沒有差異。柏拉木斑葉白區上表皮具有針束狀結晶可能也會增加光線的反射，故柏拉木斑葉的白斑為同時由上述的四種機制共同表現，Sonerila 的白區是否亦具有晶體則需再確認。此外，柏拉木葉遠軸面的氣孔數在斑葉白區顯著低於斑葉綠區和一般綠葉，且斑葉綠區的氣孔數也顯著低於一般綠葉。 柏拉木斑葉的葉綠素濃度較一般綠葉略低，可能與斑葉白區的上層葉肉組織之葉綠體較少和小有關。最大光合作用效率（Fv/Fm）之比較結果顯示斑葉的斑區與一般綠葉没有差異，但斑葉綠區顯著大於一般綠葉。在低光時（PAR < 300 μmol photons m-2 s-1），斑葉的PSII光量子產量（PSII quantum yield）和電子傳遞速率（electron transport rate, ETR）較一般綠葉低；但其非光化學消散（non-photochemical quenching, NPQ） 則較一般綠葉高，顯示斑葉的光保護能力較一般綠葉高。在高光時（PAR > 300 μmol photons m-2 s-1），斑葉的電子傳遞速率高於一般綠葉；但其非光化學消散較低，PSII光量子產量則和一般綠葉無差別。於野外測量之斑葉淨光合作用速率（Pn）顯著低於一般綠葉。 野外調查顯示柏拉木斑葉幼苗在惠蓀林場（49%）和蓮華池（61%）兩個族群的組成比率均達ㄧ半或以上，平均在第八對幼葉時由斑葉轉變為綠葉。斑葉的白斑形式由少至多可分為點狀、鏈狀和塊狀，可佔葉片1.5 - 24.8%的面積。這些白斑形式由動物視覺影像系統（AESIS）觀察模擬蜜蜂的視覺發現斑葉白區是非常明顯的。由惠蓀林場和蓮華池兩個樣區共10條樣帶各兩次的調查結果顯示柏拉木斑葉幼苗受植食性生物取食的比例顯著低於一般綠葉幼苗。柏拉木斑葉近軸面之白斑中心具有一枝明顯的多列無分枝毛，可能會影響植食者取食和降落；且其遠軸面的短柄腺毛顯著高於斑葉綠區和一般綠葉。葉片營養的分析顯示斑葉和一般綠葉之間的碳百分比、氮百分比和碳氮比皆沒有顯著差異。推測這些斑點、絨毛和草酸鈣結晶均與斑葉幼苗受植食性生物取食的比例較低有關。 本文首次報導自然斑葉的發生可導因於結構與化學機制，再加上結晶的共同作用而形成斑葉上對比?烈的白斑。柏拉木幼苗的斑葉白區和斑葉綠區與一般綠葉在多項形態和結構上的差異，因而導致斑葉在整體上因而損失若干光合作用能力，但卻可以有更好的光保護能力，並顯著地降低被取食的機會。柏拉木斑葉的出現僅幼苗最初的第七對葉子前出現，表現出斑葉幼苗異生性的適應現象。其斑葉幼苗族群的比例約維持在50%左右，且多出現在林緣環境較開闊的棲地中，推測柏拉木的斑葉現象可能在演化的過程中穩定的留存下來，並具有適應的重要意涵。
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