Trends in Plant Science

10. Yang, X. et al. (2017) 5-methylcytosine promotes mRNA

export – NSUN2 as the methyltransferase and ALYREF
of literature shows that temperature stress (Figure 1). In nature, the high demand
as an m5C reader. Cell Res. 27, 606–625 is likely to affect crop yields more nega- for replacement of the damaged D1
11. Amort, T. et al. (2017) Distinct 5-methylcytosine profiles in
poly(A) RNA from mouse embryonic stem cells and brain.
tively compared with any other stress. protein is ensured by its rapid ‘on-site’
Genome Biol. 18, 1 It has been predicted that, with every 1oC production from a highly polyploid chlo-
12. Blanco, S. et al. (2016) Stem cell function and stress
response are controlled by protein synthesis. Nature
rise in the mean global temperature, the roplast genome through one of the stron-
534, 335–340 average yield of four major field crops, gest promoters, PpsbA [6]. However,
namely maize (Zea mays), wheat (Triticum various environmental stresses, including
aestivum), rice (Oryza sativa), and soybean high temperature, reduce the capacity of
Spotlight (Glycine max), would reduce by 7.4%, chloroplasts to supply freshly synthesized
6.4%, 3.2%, and 3.1%, respectively [2]. D1 polypeptide, resulting in photoinhibition.
Such huge yield losses have been pre- Therefore, preventing PSII photoinhibition
Alternative Routes dicted to significantly impact global food has been recognized as a means of im-
to Improving security [3]. proving stress tolerance in field crops [7].
Photosynthesis in This strategy was recently explored by
Photosynthesis is a key process that Chen and colleagues [8] in three crop
Field Crops underlies both the productivity and stress species, Arabidopsis (Arabidopsis thaliana),
sensitivity of crop plants. It is one tobacco (Nicotiana benthamiana), and rice
Niaz Ahmad,1
of the most thermosensitive metabolic (O. sativa japonica).
Syed Shan-e-Ali Zaidi,2 and processes in plants and, therefore, a target
Shahid Mansoor1,* of intensive research for developing Transgenic versions of these plants were
stress-resilient yet high-yielding crop generated by expressing an Arabidopsis
Photosynthesis is an important plants [4]. When plants experience psbA gene encoding D1 polypeptide via
biochemical reaction that forms stress, their ability to fix CO2 is impaired, the nucleus under the heat inducible
the basis of all food chains. Its while their absorption of light remains un- promoter of a heat shock transcription
efficiency is considered a key affected. The excess of absorbed energy factor, AtHsfA2. To facilitate its targeting
determinant of crop productivity. results in the generation of detrimental in chloroplasts, the site of D1 assembly,
Therefore, improving photosynthetic reactive oxygen species, which can a plastid transit peptide of ribulose-1,5-
efficiency has been a focus of inten- damage the photosynthesis machinery, bisphosphate carboxylase-oxygenase
particularly photosystem II (PSII). PSII is (RuBisCo) small subunit (RbcSPTP), was
sive research. Here, we highlight
highly prone to photodamage due to the N-terminally fused with the psbA cDNA
simple approaches, recently re-
electron chemistry it performs. Plants have sequence. Analysis of the transgenic
ported by Chen et al. and Degen
evolved several mechanisms to protect plants showed that the nuclear D1 pro-
et al., to increase photosynthetic and keep PSII in an active state through tein was successfully expressed and
efficiency in field crops. an efficient repair system. Photoinhibition targeted to thylakoids. Heat treatment of
occurs when the rate of damage exceeds transgenic lines dramatically increased
The human population of the world is in- the rate of PSII repair, resulting in a psbA transcripts as well as D1 protein
creasing at an alarming rate, and, accord- reduction in photosynthetic efficiency and, compared with controls. Interestingly,
ing to United Nations estimates, will reach ultimately, reduced crop yields [5]. the increase in D1 protein also increased
a whopping ~9.7 billion people over the other components of the PSII complex,
next 30 years [1]. Therefore, feeding this While the mechanistic details of the such as D2, CP43, and CP47. Further anal-
growing population has been recognized PSII photoinhibition are still debated, yses showed that transgenic lines were
as one of the great challenges of the 21st it is generally agreed that the D1 protein, able to maintain high photosynthetic effi-
century. In the face of climate change one of the core proteins of the PSII ciency [as determined by maximum quan-
and shrinking arable land, the only option reaction center, is highly sensitive to tum efficiency of PSII (Fv/Fm)] as well as
available to meet this challenge is to photodamage. To replace damaged D1, their internal thylakoid structures under
increase crop productivity per unit area. the repair process requires partial disas- heat stress. Even under normal conditions,
A key factor currently limiting crop yields sembly of the PSII complex, removal the transgenic plant lines showed higher
is the exposure of plants to abiotic and cleavage of the damaged D1, CO2 assimilation rates, larger leaves, and
stresses, which severely impacts their insertion of the newly synthesized D1, faster growth compared with wild-type
photosynthetic capacity. A growing body and reassembly of the functional PSII plants.

958 Trends in Plant Science, October 2020, Vol. 25, No. 10

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Trends in Plant Science

Figure 1. A Simplified Scheme of Boosting the Photosystem II (PSII) Repair Cycle via Nuclear Transformation of a Chloroplast Gene, psbA, Encoding
D1. (A) The damaged PSII reaction center is repaired through an efficient repair system, which requires partial disassembly of PSII, degradation of damaged D1, insertion of
the newly synthesized D1, and then reassembly of a functional PSII complex. Under stressful environmental conditions, the PSII repair cycle is suppressed, resulting in the
photoinhibition of PSII reaction centers. (B) Chen and colleagues [8] improved PSII repair by supplying additional copies of D1 by transforming a plastid-encoded
photosynthetic gene psbA with an N-terminally fused transit peptide of small subunit of ribulose-1,5-bisphosphate carboxylase-oxygenase (RuBisCo), RbcSPTP, under
a stress inducible AtHSFA2 promoter in the nuclear genome. (C) Upon entry into the chloroplast, the transit peptide was correctly recognized and cleaved to produce a
mature D1, which was successfully incorporated into the PSII repair cycle. When plant lines expressing RbcSPTP-D1 were exposed to heat, PSII activity was
significantly increased, with a concomitant increase in photosynthetic efficiency as well as productivity.

To see whether the increased photosyn- efficiency of RuBisCo decreases with thermotolerance by 5°C of the most
thetic efficiency and CO2 assimilation increase in temperature, mainly due to abundant RCA isoform, Rca2β, found in
were translated into yield increase, the thermosusceptibility of its activator bread wheat. In addition to increasing
transgenic rice was grown in the field. protein, RuBisCo activase (RCA). While temperature optima, the M159I substitu-
These transgenic rice showed a higher RuBisCo itself is stable even up to 50oC, tion in Rca2β also increased its degree
biomass (22.3–31.7%) and grain yield per RCA activity decreases as the tempera- of sensitivity to ADP inhibition [10]. The
plant (12.8–21.0%) compared with con- ture exceeds the species-specific temper- single amino acid change provides an
trols. Thus, this simple strategy could be
ature optima for plant growth. Research excellent target to develop heat-tolerant
useful for improving crop productivity, par-
shows that expression of a thermotolerant crop plants using more efficient and
ticularly for tropical monocot and dicot version of RCA in Arabidopsis resulted in cost-effective site-directed mutagenesis
crops, in the context of global warming. a significant increase in photosynthetic techniques, such as clustered regularly
efficiency, biomass, and grain yield under interspaced short palindromic repeat/
Another highly stress-sensitive compo- moderate heat stress conditions [9]. CRISPR-associated protein 9 [11]. Recent
nent of the photosynthetic machinery Recently, in vitro assays showed that sub- improvements in CRISPR-mediated ge-
is RuBisCo, which carries out carboxyla- stitution of a single amino acid methionine nome engineering can bring several
tion of ribulose-1,5-bisphosphate in the at position 159 in the α/β subdomain by an benefits, including transgene-free crop
Calvin–Benson cycle. The carboxylation isoleucine residue, M159I, extended the production, with a higher chance of

Trends in Plant Science, October 2020, Vol. 25, No. 10 959

Trends in Plant Science

reaching farmers’ fields in time, and 2. Zhao, C. et al. (2017) Temperature increase reduces Strigolactones are a Novel Class of
global yields of major crops in four independent estimates.
the introduction of multiple useful traits Proc. Natl. Acad. Sci. U. S. A. 114, 9326–9331
Phytohormones with Diverse
simultaneously, such as disease resis- 3. Zaidi, S.S. et al. (2019) New plant breeding technologies Functions
for food security. Science 363, 1390–1391
tance, in addition to heat tolerance [12]. 4. Simkin, A.J. et al. (2019) Feeding the world: improving
SLs, a group of carotenoid-derived
photosynthetic efficiency for sustainable crop production. lactones, were initially identified as host
J. Exp. Bot. 70, 1119–1140
These two studies, by Chen et al. and 5. Ahmad, N. et al. (2020) Contrasting responses to stress
chemical cues that trigger the germination
Degen et al., provide a simple and efficient displayed by tobacco overexpressing an algal plastid ter- of seeds of root-parasitic plants, and then
minal oxidase in the chloroplast. Front. Plant Sci. 11, 501
methodology of improving an incredibly 6. Ruhlman, T. et al. (2010) The role of heterologous
as rhizosphere signals for arbuscular
complex trait, photosynthesis, in field chloroplast sequence elements in transgene integration mycorrhizal (AM) fungi to form symbiotic
and expression. Plant Physiol. 152, 2088–2104
crops to effectively address the emerging 7. Johnson, G.N. and Stepien, P. (2016) Plastid terminal ox-
interactions [1]. Since then, SLs have
global food crisis. Although there have idase as a route to improving plant stress tolerance: attracted great attention, especially in
Known knowns and known unknowns. Plant Cell Physiol.
been numerous research efforts to improve 57, 1387–1396
agriculture, due to their phytohormone
photosynthesis [4], none has been com- 8. Chen, J.H. et al. (2020) Nuclear-encoded synthesis of the roles in regulating multiple aspects of plant
D1 subunit of photosystem II increases photosynthetic
mercially successful so far. With these two efficiency and crop yield. Nat. Plants 6, 570–580
architecture, especially shoot branching,
simple techniques, crop yields can be in- 9. Kurek, I. et al. (2007) Enhanced thermostability of which is important for crop yield. SLs
Arabidopsis Rubisco activase improves photosynthesis
creased significantly. A further improve- and growth rates under moderate heat stress. Plant Cell
are also involved in regulating leaf mor-
ment in the PSII repair process could be 19, 3230–3241 phology and senescence, anthocyanin
10. Degen, G.E. et al. (2020) An isoleucine residue acts as a
possible through direct expression of thermal and regulatory switch in wheat Rubisco activase.
accumulation, photomorphogenesis, en-
D1 at the assembly site in the chloroplast Plant J. Published online May 4, 2020. https://doi.org/ dosperm development, stem secondary
10.1111/tpj.14766
using chloroplast transformation technol- 11. Ahmad, N. et al. (2020) A critical look on CRISPR-based
growth, root development, and responses
ogy. In nature, D1 is expressed by the chlo- genome editing in plants. J. Cell. Physiol. 235, 666–682 to various stresses [1].
12. Zaidi, S.S. et al. (2018) Genome editing: targeting suscepti-
roplast genome, where its synthesis is bility genes for plant disease resistance. Trends Biotechnol.
coupled with the degradation and removal 36, 898–906 Studies with more branching (or tillering)
of damaged D1 (Figure 1). Work from vari- and dwarf mutants in arabidopsis
ous laboratories shows that transformation (Arabidopsis thaliana), rice, pea, and petunia
of the chloroplast genome allows the ex- identified conserved components in SL
biosynthesis and signaling. SLs
pression of recombinant proteins at much
increased levels. Therefore, direct expres-
Spotlight are synthesized from β-carotene by
sion of D1 protein in chloroplast would en- sequential reactions catalyzed by β-
sure a quick and efficient supply of the Strigolactone Signaling: carotene isomerase, carotenoid cleavage
dioxygenase 7 (CCD7), CCD8, and cy-
protein in large amounts at the site where Repressor Proteins Are tochrome P450 monooxygenase [2].
it is needed. Unfortunately, this technology
is currently restricted to a few crop species
Transcription Factors SLs are sensed by the α/β hydrolase
and remains challenging to use in mono- DWARF14 (D14), a dual-functional re-
Jiuyou Tang1,* and ceptor responsible for both the percep-
cots, which comprise most of the staple
Chengcai Chu 1,* tion and hydrolysis of SLs [3]. In the
food crops consumed worldwide.
presence of SLs, D14 interacts with
1
Agricultural Biotechnology Division, National Institute for its respective F-box protein, such as
Biotechnology and Genetic Engineering (NIBGE), Faisalabad, A recent landmark study by MORE AXILLARY GROWTH2 (MAX2) in
38000, Pakistan
2
Gembloux Agro-Bio Tech, University of Liège, Gembloux 5030,
Wang et al. provides new insight arabidopsis and DWARF3 (D3) in rice,
Belgium into transcriptional regulation in from a SKP1-Cullin-F-box complex (SCF),
*Correspondence:
strigolactone (SL) signaling. The and recruits repressor proteins, such as
[email protected] (S. Mansoor). finding that SUPPRESSOR OF SUPPRESSOR OF MAX2 LIKE (SMXL) 6,
https://doi.org/10.1016/j.tplants.2020.07.003 MAX2 LIKE 6 (SMXL6) also func- SMXL7, and SMXL8 (SMXL6,7,8 hereafter)
© 2020 Elsevier Ltd. All rights reserved. tions as an autoregulated transcrip- in arabidopsis and DWARF53 (D53) in
rice, for ubiquitination and degradation
tion factor (TF) causes a paradigm
References [2–6]. The F-box protein D3 can switch
shift in the current view of transcrip-
1. Population Facts (2019) How certain are the United between two conformation states via its
Nations global population projections?, Population Division tional repressors in phytohormone C-terminal α-helix, and this structural plas-
of the United Nations, Department of Economic and Social
Affairs, pp. 1–4 signaling. ticity has a key role in the coordination of SL

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